Nitrogen dynamics in the Caatinga Rômulo S. C. Menezes, Ph. D.

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Nitrogen dynamics in the Caatinga Rômulo S. C. Menezes, Ph. D. Associate Professor, Universidade Federal de Pernambuco E-mail: romuloscmenezes@gmail.com

Main topics to be discussed Introduction about Caatinga N stocks and impacts of land use and climate change N cycling and management strategies in low input systems Guiding questions Summary and conclusions

Description of the Caatinga ecosystem Land cover in the Caatinga Biome Area (Millions ha) % Native vegetation 44,1 53,38 Deforested area (pastures and agriculture) 37,9 45,92 Water 0,83 1,01 Total 84,44 100 Same area of Germany and Spain combined Population: about 25 million people Land tenure: Majority of farms smaller than 10 ha Source: http://siscom.ibama.gov.br/monitorabiomas/ Lowest human development index in Brazil

High variability of rainfall precipitation Average annual precipitation: 300 to 800 mm in different areas of the region; On average, 60% of the rainfall in one month, while 30% happens in a single day; In the long term: Severe droughts have occurred every 10 to 15 years.

High variability of soil types Mostly shalow soils Rich in bases (K, Ca, Mg) Low organic matter Low N and P availability

Main land use types in the Caatinga Biome Subsistence agriculture (maize, beans and cassava) Livestock production (cattle, goats, and sheep grazing on caatinga vegetation) Wood extraction from caatinga

THE LANDSCAPE Small farms divided in patches of agricultural fields, pastures and native vegetation Patches of native vegetation in more advanced succession stages Patches of disturbed native vegetation Patches of agricultural fields and pastures

Mature, well preserved caatinga vegetation (Patos, PB)

Soil N stocks in the top layer(0-20 cm) in diferent Brazilian ecosystems Biome Soil N stocks in top layer (t ha -1 ) Mata Atlântica 14-20 Cerrado 4,6 Caatinga 2,5 Source: Martinelli et al., 2014 (Chapter 5, PBMC, 2014) Lower stocks in Caatinga compared to other ecosystems

Quantification of C and N stocks in caatinga-study sites 0-10 10-20 20-30 30-40 40-60 60-80 80-100

Nitrogen stocks (t ha -1 ) Nitrogen stocks in a preserved Caatinga site (mature, dense native vegetation, 0-100 cm soil layer) 12.00 Soil Belowground biomass Aboveground biomass 10.00 9.6 t ha -1 Above ground plant N: 0.58 t ha -1 (6 % of the N stock) 8.00 Root N: 0.29 t ha -1 (3 % of the N stock) 6.00 4.00 Soil N: 8.8 t ha -1 (91% of the system N stock) 2.00 0.00 Mature caatinga Disturbed caatinga Pasture Agriculture

Nitrogen stocks (t ha -1 ) Nitrogen stocks in different land use systems in the Caatinga (0-100 cm soil layer) 12.00 Soil Belowground biomass Aboveground biomass 10.00 8.00 Losses of 3.3 t of N (34%) Losses of 3.4 t of N (36%) Losses of 4.4 t of N (46%) 6.00 4.00 2.00 0.00 Mature caatinga Disturbed caatinga Pasture Agriculture Losses of 3000 to 4000 kg N ha -1 Remember these numbers!!

Drivers of land use change and N dynamics An important driver for N fluxes in the caatinga: grazing

The leather civilization The importance of livestock production in the caatinga

Livestock expansion in the Caatinga Sugarcane cultivation in the humid coastal area since the 1600 s Portuguese crown prohibition of cattle in the sugarcane area High demand for leather and meat Availability of large areas of range suitable for cattle in the Caatinga region Land leasing from the crown and labor arrangements with vaqueiro system

Typical farmhouse in the caatinga With the corral next to the house

The importance of cattle in the Caatinga Livestock production, due to the pattern of colonization of the region, is a very importante activity, both from the cultural and socioecnomic point of view. For this reason, today we observe very high animal stocking rates in most of the region (i.e., more animals than the land could sustainably support).

Guiding questions - What are the relative roles roles of industrial N, biological N fixation, and organic N recycling in optimizing N use?

Nitrogen cycling in the Caatinga ecosystem Management strategies Few N inputs X Fertilizer purchase Atmospheric deposition Harvest Slash and burn N 2 fixation Uptake Plants Grazing Crop residues Litterfall Herbivores Sale Emissions Deposition Deposition Corral (manure) Sale Emissions Fertilization Emissions Soil surface layer Leaching Soil erosion Runoff Input fluxes: blue arrows Output fluxes: red arrows Internal cycling: green arrows Adapted from Menezes et al. (2012)

Atmospheric N deposition (2 studies published) Deusdará, K.R.L., Forti, M.C., Borma, L.S. Menezes, R. S. C., Lima, J. R. S., Ometto, J. P. H. B. Rainwater chemistry and bulk atmospheric deposition in a tropical semiarid ecosystem: the Brazilian Caatinga. J Atmos Chem (2016). doi:10.1007/s10874-016-9341-9 MARIN, A. M. P., Menezes, R. S. C. Ciclagem de nutrientes via precipitação total, interna e escoamento pelo tronco em sistema agroflorestal com Gliricidia sepium. Revista Brasileira de Ciência do Solo, v.32, p.2573-2579, 2008. About 2 to 5 kg ha -1 year -1

Nitrogen cycling in the Caatinga ecosystem Atmospheric deposition Fertilizer purchase Harvest Slash and burn N 2 fixation Uptake Plants Grazing Crop residues Litterfall Herbivores Sale Emissions Deposition Deposition Corral (manure) Sale Emissions Fertilization Many processes causing N outputs Emissions Soil surface layer Leaching Soil erosion Runoff Input fluxes: blue arrows Output fluxes: red arrows Internal cycling: green arrows Adapted from Menezes et al. (2012)

Main N losses from the system: How to mitigate it? Slash and burn: N losses up to 500 kg ha -1 during burning of dense, mature native vegetation; It is necessary about 20 to 30 years of biological N fixation to recover it; What to do? No biomass should be burned. Erosion: N losses due to soil erosion could be generally up to 30 to 40 kg ha -1 year -1 in agricultural fields; Pastures could also present intermediate to high erosion rates; What to do? Soil erosion control measures must be implemented, otherwise N balance will be negative. Emissions: N losses due to soil emissions are relatively low (~1 kg ha -1 year -1 ) (Ribeiro et al., 2016); More studies are needed.

Guiding questions - What are is the balance between fixation, immobilization and decomposition (losses) in the N cycle under different management and in different environments?

Quantification of nutrient fluxes and balances in six farms in NE Brazil during two years Pasture Caatinga Sales of animals, grains, milk and manure Garden Corral Croping field House

Average net nutrient balances in agricultural fields and pastures in six farms in the caatinga during two years (kg ha -1 year -1 ) Land use Nitrogen Phosphorus Potassium Agriculture -16-1 -18 Pasture - 3-0.1-4 Balances in native vegetation plots were positive for nitrogen and near zero for P and K. A great amount of the nutrients removed from agricultural fields and pastures end up in the corral Average manure sales (per farm): ~ 100, 40 e 150 kg year -1 of N, P and K

Nitrogen cycling in the Caatinga ecosystem How to bring N into the system in a sustainable way? X Atmospheric deposition Fertilizer purchase Harvest Slash and burn N 2 fixation Uptake Plants Grazing Crop residues Litterfall Herbivores Sale Emissions Deposition Deposition Corral (manure) Sale Emissions Fertilization Emissions Soil surface layer Leaching Soil erosion Runoff Input fluxes: blue arrows Output fluxes: red arrows Internal cycling: green arrows Adapted from Menezes et al. (2012)

Estimates of biological nitrogen fixation (BNF) in mature and regenerating caatinga areas MATURE VEGETATION REGENERATING VEGETATION Site 1 Site 2 Site 1 Site 2 Proportion of N fixers (%) 2,4 11,8 58 97 Mass of N fixers (kg) 170 625 1620 1310 Amount of N fixed (kg/ha) 3 11 26 21 MATURE CAATINGA 7 kg ha -1 year -1 REGENERATING CAATINGA 23 kg ha -1 year -1 Fonte: Freitas e Sampaio, 2008

Guiding questions - What are the limitations of biological N fixation under climate stress and under climate change? Low water and P availability limit BNF. Climate change will make it worse.

Traditionally, soil fertility recovery was done through rotation of cropping areas and recovery of native vegetation during fallow periods. Fallow periods are too short nowadays.

Litter N content in different successional stages of caatinga Greater ammounts in intermediate stages

Carbon and nutrient recovery along a succession gradiente of caatinga regeneration Up to 57 years of regeneration Around 40% of increase in C and N levels Increase of 1200 kg ha -1 in 57 years Net increase of 21 kg N ha -1 year -1

Just do the math: N inputs due to BNF + atmospheric deposition ~ 25 to 30 kg ha -1 Conversion of native forest to agriculture = losses of 3000 to 4000 kg N ha -1 Time to recover original ecosystem N stocks = 100 to 150 years! Actual falow periods = 10 to 15 years... End result = soil fertility degradation, lower productivity, poverty, more degradation.

Carbon and nitrogen dynamics after land use change in the caatinga Althof et al. (2016) Aboveground Vegetation N Stock Soil Nitrogen Mg N ha -1 0.3 0.25 0.2 0.15 0.1 0.05 0 1950 1960 1970 1980 1990 2000 2010 Years 3.5 3 2.5 2 1.5 1 0.5 0 1950 1960 1970 1980 1990 2000 2010 Years

Regeneration of vegetation under current or projected climate changes Current climate Projected scenarios Mg N ha -1 Aboveground Nitrogen Stocks Soil Nitrogen (top layer) 0.3 0.25 0.2 0.15 0.1 0.05 0 2000 2010 2020 2030 2040 2050 2060 2070 2080 2090 2100 Years 3.5 3 2.5 Plant and soil N never return to original stocks even after 100 years 2 2000 2010 2020 2030 2040 2050 2060 2070 2080 2090 2100 Years

Guiding questions - What innovative strategies for N management exist using plant breeding, microbial associations, fertilizer formulations and others?

Nitrogen cycling in the Caatinga ecosystem Harvest Slash and burn Sale Emissions Some crops and legume species used as green manure may fix up to 40 to 50 kg ha -1 year -1 of nitrogen (and up to 180kg in irrigated plots). Atmospheric deposition Fertilizer purchase N 2 fixation Uptake Plants Grazing Crop residues Litterfall Herbivores Deposition Soil surface layer Leaching Deposition Corral (manure) Sale Emissions Fertilization Emissions Soil erosion Runoff TAKE HOME MESSAGES: 1) Atmospheric N fixation is the most feasible way to bring significant amounts of N into the system; 2) Very disturbed systems may require decades to over a century to recover natural fertility levels (if ever). 3) In some cases, therefore, external input of N may be necessary to recover the system. Adapted from Menezes et al. (2012)

Agroforestry Systems Alley cropping Mixed systems Silvopastoral systems

Nitrogen cycling in the Caatinga ecosystem Harvest Slash and burn Sale Emissions Atmospheric deposition Fertilizer purchase Uptake N 2 fixation Uptake Plants Grazing Crop residues Litterfall Herbivores Deposition Deposition Corral (manure) Sale Emissions Fertilization Emissions Soil surface layer Leaching Soil deeper layers Soil erosion Runoff Input fluxes: blue arrows Output fluxes: red arrows Internal cycling: green arrows Adapted from Menezes et al. (2012)

Profundidade (cm) Trees may tap nutrients (and water) from deeper soil layers Access tubes 0 m 1 m 3 m Agua em contagem relativa (CR) 0,00 0,20 0,40 0,60 0 20 40 60 Gliricidia trees took up water and nitrogen from 120-150 cm of depth. Maize plants were not able to reach these resources. 80 100 120 140 160 Injection of 15 N Agroforestry systems: 150% more biomass production than maize plots without trees 180 SA CA0m CA1m CA3m

Nitrogen cycling in the Caatinga ecosystem Harvest Slash and burn Sale Emissions Atmospheric deposition Fertilizer purchase Uptake N 2 fixation Uptake Plants Grazing Crop residues Litterfall Herbivores Deposition Deposition Corral (manure) Sale Emissions Fertilization Emissions Soil surface layer Leaching Soil deeper layers Soil erosion Runoff Input fluxes: blue arrows Output fluxes: red arrows Internal cycling: green arrows Adapted from Menezes et al. (2012)

Organic fertilization (Green and animal manures) Up to 10 times more productivity with adequate practices of organic fertilization

Fertilization practices to sinchronize plant demand and soil N availability N release: 100% of fertilizer at planting N release: Splitting fertilizer at planting and 40 DAP Maize N accumulation in fertilized plants (~50 kg ha -1 ) Maize N accumulation in plants without fertilization

Strategies for synchronization Manure accumulates in the corral during the dry season; Biomass from green manure species sprout during the rainy season and need time to accumulate biomass; Based on this, manure should be incorporated before planting and green manure should be surface applied during the crop cycle, right before the period of higher nutrient demand. Composting, if possible, could also be done before the planting season and applied during planting. Manure - Slow N release (must avoid immobilization) Rains and planting Green manure Fast N release Period of higher crop nutrient demand

Guiding questions What is the role of public and private sector policy in improving N management? Public policies and education to promote more adapted nutrient management practices.

Summary and conclusions N stocks in soils and vegetation are low, due to the low and variable precipitation; Nitrogen and phosphorus and are the most limiting soil nutrients in the caatinga; Use of fertilizers and irrigation not feasible in most of the Caatinga; BNF is the most sustainable way of adding N to the system; Control of processes that lead to N losses is crucial to maintain positive N balances; Need for more research on N emissions; Degraded systems may require over 100 years of BNF to recover natural N stocks; Agroforestry and use of organic fertilizers increase ecosystem productivity; Need for effective policies to promote sustainable nutrient management.

References ALTHOFF, TIAGO DINIZ, Menezes, Rômulo Simões Cezar, DE CARVALHO, ANDRÉ LUIZ, DE SIQUEIRA PINTO, ALEXANDRE, SANTIAGO, GABRIELA AYANE CHAGAS FELIPE, OMETTO, JEAN PIERRE HENRY BALBAUD, VON RANDOW, CELSO, DE SÁ BARRETTO SAMPAIO, EVERARDO VALADARES. Climate change impacts on the sustainability of the firewood harvest and vegetation and soil carbon stocks in a tropical dry forest in Santa Teresinha Municipality, Northeast Brazil. Forest Ecology and Management. v.360, p.367-375, 2016. Menezes, RSC, Sampaio, EVSB, Giongo, V, Pérez-Marin, AM. Biogeochemical cycling in terrestrial ecosystems of the Caatinga Biome. Brazilian Journal of Biology, v.72, p.643-653, 2012. COSTA, TÂNIA L., Sampaio, Everardo V. S. B., SALES, MARGARETH F., ACCIOLY, LUCIANO J. O., ALTHOFF, TIAGO D., PAREYN, FRANS G. C., ALBUQUERQUE, ELIZA R. G. M., Menezes, Rômulo S. C. Root and shoot biomasses in the tropical dry forest of semi-arid Northeast Brazil. Plant and Soil (Print), v.378, p.113-123, 2014. Souza, Leonardo Queiroz, Freitas, Ana Dolores Santiago, Sampaio, Everardo Valadares de Sá Barretto, Moura, Patrícia Maia, Menezes, Rômulo Simões Cezar. How much nitrogen is fixed by biological symbiosis in tropical dry forests? 1. Trees and shrubs. Nutrient Cycling in Agroecosystems, v.94, p.171-179, 2012. Freitas, Ana Dolores Santiago, Sampaio, Everardo Valadares Sá Barretto, SILVA, BÁRBARA LAINE RIBEIRO, ALMEIDA CORTEZ, JARCILENE SILVA, Menezes, Rômulo Simões Cezar. How much nitrogen is fixed by biological symbiosis in tropical dry forests? 2. Herbs. Nutrient Cycling in Agroecosystems., v.of, p.1-12, 2012. MARTINS, J. C.R., FREITAS, A.D.S., MENEZES, R. S. C., SAMPAIO, E. V. S. B. Nitrogen symbiotically fixed by gliricidia and cowpea in an agroforestry system in semiarid Northeast Brazil. Pesquisa Agropecuária Brasileira (1977. Impressa). v.50, p.178-184, 2015. RIBEIRO, KELLY; SOUSA-NETO, ERÁCLITO RODRIGUES DE; CARVALHO, JOÃO ANDRADE DE; SOUSA LIMA, JOSÉ ROMUALDO DE; Menezes, Rômulo Simões Cezar; DUARTE-NETO, PAULO JOSÉ; DA SILVA GUERRA, GLAUCE; OMETTO, JEAN PIERRE HENRY BAULBAUD. Land cover changes and greenhouse gas emissions in two different soil covers in the Brazilian Caatinga. Science of the Total Environment., p.1-8, 2016. DOI: doi:10.1016/j.scitotenv.2016.07.095 SANTOS, MAURO G., OLIVEIRA, MARCIEL T., FIGUEIREDO, KARLA V., FALCÃO, HIRAM M., ARRUDA, EMÍLIA C. P., ALMEIDA-CORTEZ, JARCILENE, Sampaio, Everardo V. S. B., OMETTO, JEAN P. H. B., Menezes, Rômulo S. C., OLIVEIRA, ANTÔNIO F. M., POMPELLI, MARCELO F., ANTONINO, ANTÔNIO C. D. Caatinga, the Brazilian dry tropical forest: can it tolerate climate changes?. Theoretical and Experimental Plant Physiology, v.26, p.83-99, 2014. PBMC, 2014: Base científica das mudanças climáticas. Contribuição do Grupo de Trabalho 1 do Painel Brasileiro de Mudanças Climáticas ao Primeiro Relatório da Avaliação Nacional sobre Mudanças Climáticas [Ambrizzi, T., Araujo, M. (eds.)]. COPPE. Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brasil, 464 pp.