Phosphorus in agroforestry systems: a contribution to sustainable agriculture in the Zona da Mata of Minas Gerais, Brazil

The Zona da Mata is a region situated in the domain of the Atlantic Coastal Rainforest in the southeast of the state of Minas Gerais, Brazil. This domain stretches along the Brazilian coast from north to south and ranks among the top five of the 25 biodiversity hotspots, the richest and the most threatened reservoirs of plant and animal life on Earth. Originally, forest covered the region but nowadays only about 7.5 % of the original vegetation remains. Most of the trees were cut for wood and the area is nowadays used for agriculture. In general, the agro-ecosystems in the Zona da Mata show a decreasing productivity due to the increasing intensity of soil use, with practices inadequately adapted to the environment. In 1993, farmers and researchers searching for a more sustainable agriculture started implementing or improving agroforestry coffee (cash-crop) systems in the region. The natural environmental conditions of the region are favourable for growing trees, as illustrated by the fact that the entire area was originally covered with forest. The main goals with agroforestry were 1) land regeneration and conservation; 2) decrease of external input to agriculture; 3) increase or maintenance of production level; and 4) improvement of productivity. To reach these goals, a better understanding of nutrient recycling in the systems is required. The work presented here aims to contribute to such better understanding and focuses on the effect of agroforestry on phosphorus (P) cycling. Phosphorus may be the major nutrient in relatively short supply in mos t natural ecosystems, and the primary limiting nutrient for crop production in highly weathered tropical soils. The P deficiency is mainly caused by strong adsorption of H 2 PO 4-to aluminium (Al) and iron (Fe) (hydr)oxides, which turn large proportions of total P into a form that is unavailable to plants. The main strategy to cope with P deficiency in the tropics has been the addition of fertilisers. At the same time, the global reserves of apatite, which is needed for producing P fertilisers, are limited and known reserves may be exhausted in about 100 years with the current growth of P usage. More sustainable strategies need to be developed to utilise applied and native soil P more effectively to reduce P fertiliser demands. Agroforestry can be considered one of these strategies. The main hypothesis was that in agroforestry systems, part of the unavailable inorganic P (Pi) in soil is made available to agricultural crops by modifying P dynamics along various pathways. Some tree roots can use more soil than crop roots, have different associations with micro-organisms including mycorrhiza and change the rhizosphere through exudates, such as organic anions and phosphatase. The core questions of this thesis were: a) Do agroforestry systems modify P dynamics in the soil? b) Do these modifications vary with depth? c) Do agroforestry systems increase P cycling release P that is otherwise unavailable to the crops? d) How does this process occur?To answer these questions, I characterised soils under agroforestry and conventional (full-sun, monoculture) coffee systems from the Zona da Mata of Minas Gerais at different depths and studied mechanisms involved in the improvement of P recycling. The outline of the research, as well as the description of the problem and area were presented in Chapter 1. Chapter 2 described the participatory processes and range of methods by which agroforestry systems took hold in the Zona da Mata. It discussed some of the key benefits and problems of agroforestry systems encountered during the first five years. Chapter 2 also showed how the starting point of the research questions presented in this thesis emerged from the participatory monitoring and evaluation of the agroforestry systems in Araponga, Zona da Mata.A first step in the study of P dynamics is the estimation of the various P pools in the soil, including organic P, which is usually done by P fractionation. With the P fractionation procedures (Chapter 3), I showed differences between agroforestry and conventional systems: the amount of organic P (Po) decreased less with depth (effect of depth in the Sum-Po) and the percentage of organic P in labile pools was higher (effect of systems in the Sum-Po : labile) in the agroforestry fields. In Chapter 4 I used 31PNMR (phosphorus 31 nuclear magnetic resonance) to evaluate the inorganic (Pi) and organic P (Po) compounds in the soils. The results confirmed and extended the results of the previous chapter. I found that the ratios of organic P to total P and of diester (a labile Po compound) to total P are higher in agroforestry coffee fields than in conventional coffee fields. There were also effects of depths: agroforestry fields showed a higher ratio of organic P to total P in depth than conventional coffee fields. Moreover, the amount of diester and the ratio diester : monoester (a less labile Po compound) decreased less with depth in the agroforestry fields than in the conventional fields. These results are consistent with the hypothesis that agroforestry systems influence the dynamics of P through the conversion of part of the inorganic P into organic P, which is probably a consequence of higher biological activity in the agroforestry systems. Because organic P appear to be less readily fixed than inorganic forms and because soil biological activity is likely to lead to greater recycling into younger, more labile, P pools agroforestry would maintain higher fractions of P available to agricultural crops and would reduce P losses to the unavailable pools.In Chapter 5, I reported on the presence of higher numbers of spores of arbuscular mycorrhizal fungi (AMF) in the deeper soil layers of the agroforestry fields than in the deeper soil layers of the conventional fields. This was probably due to the presence of more roots in deep layers in the agroforestry fields than in the conventional fields. The presence of more spores may be an indicator of higher incidence of mycorrhiza in deeper layers of agroforestry fields than in conventional fields. High activity of mycorrhiza (in deep layers) may increase P recycling from the deeper layers in the agroforestry fields and may change the dynamics of P in the soil, for instance through changing the distribution of P over the various pools (Chapters 3 and 4). The effects of agroforestry systems, mainly in depth, found in Chapters 3 and 4 are in line with the findings in Chapter 5.In Chapter 6, I studied one of the mechanisms that plants can use to cope with P deficiency in acid soils, i.e. the association with mycorrhiza. I used an Al-resistant maize variety. In this experiment I merged the double pot, normally used in plant nutrition experiments, with the double compartment approach, normally used in mycorrhizal experiments. The mycorrhizal plants grew better in the acid soil than the non-mycorrhizal plants. The mycorrhizal plants depleted P from the readily labile fractions (Resin and NaHCO 3 -Pi) and acquired about 20 % of the moderately (NaOH-Pi) labile fractions whereas the non-mycorrhizal plants failed completely in acquiring P even from the labile fractions. It is currently accepted that mycorrhizal plants acquire P from the same source of available P as non-mycorrhizal plants but mycorrhizas explore more volume of soil than roots. Although controversial, it has also been suggested that mycorrhiza may benefit plant growth by increasing the availability of P from non-labile sources. In my experiment, mycorrhiza did more than just increase the soil volume explored by the roots. Furthermore, I also showed that the double pot - double compartment approach was suitable for the study of nutrient uptake by mycorrhiza and subsequent transfer to the plants.Chapter 7 is a summary of Chapter 6, emphasising that mechanisms of Al resistance and P uptake from soil with high Al toxicity are not necessarily related, contrary to what is commonly assumed. The Al resistance was probably due to the production of high amounts of citric acid by the maize variety. Current knowledge suggests that this mechanism also facilitates P uptake from acidic soils. However, the roots from the Al-resistant variety failed to acquire P from the soils in the absence of mycorrhizas, even from readily available fractions in the A horizon (Resin and NaHCO 3 -Pi). Therefore, the mechanisms to cope with Al toxicity and P deficiency were not necessarily interrelated, contrary to suggestions from the literature. If citric acid plays a role in the Al resistance of this variety, it is not important for direct P acquisition.In Chapter 8, the model (based on DYNAMITE model) developed as an exercicise to study P cicle, qualitatively confirmed the results from Chapter 3 that the ratio Po to labile P is higher in agroforestry than in conventional systems. The exercise was useful in integrating information. Missing information also come to light, mainly the role of the micro-organisms in the P flows among pools.Results of the P fractionation of the soil (Oxisol) used in the greenhouse experiment (Chapter 6) confirmed the results of the P fractionation of the soils (also Oxisols) from the agroforestry and conventional coffee systems (Chapter 3): the amount of total P in the soils used in the greenhouse experiment (Chapter 6) was not very low, however, on average 70 % of P was in the concentrated HCl and residue fractions, which are considered unavailable to plant crops in the short (one season) or medium term (more than one season); and the second highest fraction consisted of NaOH-Pi pool (on average 25 %), which is considered available in the medium term. Diffusion is the main mechanism of P transport in soil. Thus, in the long term, the use of NaOH-Pi and the readily available fractions (Resin-Pi and NaHCO 3 -P) by mycorrhiza (Chapter 6), will shift the partitioning of P between pools.Thus, if trees can change the performance of mycorrhiza in the agroforestry systems as compared to the conventional systems, for instance by increasing the activity of mycorrhiza in deeper layers (presence of more spores, Chapter 5), I would expect a change in P dynamics that would make more P available to the plant. This would increase the efficiency of nutrient recycling processes in the agroforestry systems.The rate and the impacts of this change on P cycling and the efficiency of P use of the crops in the long term needs to be further examined and understood before coming to a comprehensive evaluation of the importance of agroforestry in soil P utilisation. Some of the methods used in this thesis (P fractionation and 31PNMR analysis) are too static to study P dynamics and are insufficient to draw final conclusions on P transformations. Spore number (Chapter 5) is only an indicator of mycorrhiza presence. Mechanisms of P acquisition have to be understood not only in crop plants (maize for instance, Chapters 6 and 7) but also in the native trees used in the agroforestry systems, such as the trees listed in Chapters 2 and 5. Thus, detailed studies are required for a better understanding of the P transformation in soil through microbial activity. The results of these studies can be incorporated in the model (Chapter 8) to improve it.This study forms a starting point to understand P dynamics in the agroforestry systems in the Zona da Mata of Minas Gerais. The farmers request for more insight into nutrient dynamics (Chapter 2) cannot be answered completely yet. To do so, P studies must be integrated into existing agricultural development activities that are being carried out by the key players in the Zona da Mata: farmers, staff from CTA (Alternative Technologies of the Zona da Mata), researchers from UFV (Federal University of Viçosa), among others. In Chapter 9, I discussed some of the research that has been done on the agroforestry systems in the Zona da Mata and I proposed a framework for my future research on P cycling in these systems. These suggestions will also be relevant for other regions of the Atlantic Coastal Rainforest.