Effect of ecological and conventional managements on soil enzymatic activities in coffee agroecosystems

Efeito de manejos ecológico e convencional sobre atividades enzimáticas do solo em agroecossistemas cafeeiros

Johana Juliet Caballero Vanegas Karen Bibiana Mejía Zambrano Lizeth Manuela Avellaneda-Torres About the authors

ABSTRACT

Understanding the impacts of agricultural practices on soil quality indicators, such as enzymatic activities, is of great importance, in order to advance in their diagnosis and sustainable management. This study aimed to evaluate the effect of ecological and conventional agricultural managements on enzymatic activities of a soil under coffee agroecosystems. The enzymatic activities were associated with the biogeochemical cycles of nitrogen (urease and protease), phosphorus (acid and alkaline phosphatase) and carbon (β-glucosidase), during the rainy and dry seasons. Physical-chemical soil proprieties were also assessed and related to resilience scores linked to the climatic variability reported for the areas under study. The activities of urease, alkaline and acid phosphatase and ß-glucosidase were statistically higher in ecological agroecosystems than in conventional ones. This may be attributed to the greater application of organic waste in the ecological environment, as well as to the absence of pesticides and synthetic fertilizers, which allow better conditions for the microbial activity. The resilience scores to the climate variability that showed the highest correlations with the assessed enzymatic activities were: the farmers' knowledge on soil microorganisms, non-use of pesticides and synthetic fertilizers and non-dependence on external supplies. It was concluded that the enzymatic activities are modified by the management systems, being specifically favored by the ecological management. This agroecosystem, in the long term, ensures an efficient use of the soil resources, with a lower degradation and contamination.

KEYWORDS:
Urease; protease; β-glucosidase; acid and alkaline phosphatase

RESUMO

Compreender os impactos de práticas agrícolas sobre os indicadores de qualidade do solo, como atividades enzimáticas, é de grande importância para avançar no diagnóstico e no manejo sustentável. Objetivou-se avaliar o efeito dos manejos agrícolas ecológico e convencional sobre as atividades enzimáticas de um solo em agroecossistemas sob cultivo de cafeeiro. As atividades enzimáticas foram associadas aos ciclos biogeoquímicos do nitrogênio (urease e protease), fósforo (fosfatase ácida e alcalina) e carbono (β-glicosidase), durante as estações chuvosa e seca. Propriedades físico-químicas do solo também foram avaliadas e relacionadas a escores de resiliência vinculados à variabilidade climática reportada para as áreas em estudo. As atividades de urease, fosfatase alcalina e ácida e ß-glicosidase foram estatisticamente maiores nos agroecossistemas ecológicos do que nos convencionais. Isto pode ser atribuído à maior aplicação de resíduos orgânicos no manejo ecológico, bem como à ausência de pesticidas e fertilizantes sintéticos, o que possibilita melhores condições para a atividade microbiana. Os escores de resiliência à variabilidade climática que mostraram as maiores correlações com as atividades enzimáticas avaliadas foram: conhecimento dos agricultores sobre micro-organismos do solo, não uso de agrotóxicos e fertilizantes sintéticos e não dependência de insumos externos. Concluiu-se que as atividades enzimáticas são modificadas pelos sistemas de manejo, sendo especificamente favorecidas pelo manejo ecológico. Este agroecossistema, a longo prazo, assegura o uso eficiente dos recursos do solo, com menor degradação e contaminação.

PALAVRAS-CHAVE:
Urease; protease; β-glucosidase; fosfatase ácida e alcalina

INTRODUCTION

Soil is the basis for agriculture and terrestrial ecosystems, and life on the planet depends on it. It is a living, dynamic and non-renewable natural resource, and its functioning is key for the production of food and for the maintenance of environmental quality (Ochoa et al. 2007OCHOA, V. et al. Actividades enzimáticas como indicadores de calidad del suelo en agroecosistemas ecológicos. Iniciación a la Investigación, v. 2, n. 1, p. 1-10, 2007.).

Conventional agriculture has demonstrated a capacity for production and profitability in the short term; however, resources such as soil, water and genetic diversity have been overused. As a result, soils have been salinized due to excessive irrigation with low quality water containing salts, compacted by excessive tillage, leading to a loss of permeability and increase in runoff, contamination by pesticides and heavy metals, reduction of structural quality due to loss of organic matter, loss of fertility and increase of erosion (Gliessman 2002GLIESSMAN, S. Agroecología: procesos ecológicos en agricultura sostenible. Turrialba: Catie, 2002.). In addition, the release of greenhouse gases and the eutrophication of rivers, streams, lakes and coastal and marine ecosystems are also consequences of a bad soil management.

As a response to the degradation of natural resources associated with conventional agriculture, ecological agriculture has emerged, which belongs to the so-called alternative agricultures. It rejects the use of pesticides for the management of insects and diseases, seeks to increase the soil fertility and to prevent the degradation of its structure, avoids any type of contamination, prioritizes policrops on crops and seeks the integrated management of the agroecosystem (Peris et al. 2000PERIS, M. et al. La calidad de las prácticas agrícolas en el proceso de transformación a la agricultura ecológica en Enguera y Anna (Comunidad Valenciana). Cuadernos Geográficos de la Universidad de Granada, v. 31, n. 1, p. 129-147, 2000.). As their components are integrated, the general biological efficiency is increased, and the productive and self-sufficient capacity of the agroecosystem is maintained (Altieri 2001ALTIERI, M. Agroecología: principios y estrategias para diseñar sistemas agrarios sustentables. In: SARANDÓN, S. (Ed.). Agroecología: el camino hacía una agricultura sustentable. La Plata: Ediciones Científicas Americanas, 2001. p. 49-56.).

The indicators of soil quality can be physical, biological or chemical, and, considering the enzymatic activity, they can also be biochemical (Avellaneda-Torres 2008AVELLANEDA-TORRES, L. M. Actividades enzimáticas de suelos con y sin historia de uso agrícola y manejo convencional y de sus consorcios bacterianos. 2008. 208 f. Thesis (M.Sc. in Chemical Science) - Universidad Nacional de Colombia, Colombia, 2008.). Soil enzymatic activities have been suggested as a potential within the set of indicators, due to their relationship with the soil biology, since their presence depends directly on the continuous release carried out by the organisms that inhabit the ecosystem (Albiach et al. 2006ALBIACH, R. et al. Sobre las enzimas del suelo y sus técnicas de medida. Edafología, v. 13, n. 3, p. 117-125, 2006.). Likewise, the enzymatic activity in cultivated soils is also related to cultivation practices and may be directly associated with the availability of nutrients, since nutrients play important roles in each biogeochemical cycle of elements required for plant growth (Torres & Lizarazo 2006TORRES, M.; LIZARAZO, L. Evaluación de grupos funcionales (ciclo del C, N, P) y actividad de la fosfatasa ácida en dos suelos agrícolas del departamento de Boyacá (Colombia). Agronomía Colombiana, v. 24, n. 2, p. 317-325, 2006.). In some scenarios, it has been suggested that organic amendments increase the activity of enzymes in the soil (Martens et al. 1992MARTENS, D. A.; JOHANSON, J. B.; FRANKENBERGER JUNIOR, W. T. Production and persistence of soil enzyme with repeated addition of organic residues. Soil Science, v. 153, n. 1, p. 53-61, 1992.) in the same way that the use of organic amendments (slurry, composting, bokashi) stimulate the microbial life in the soil and the nutrition of the plants. On the other hand, Pascual et al. (2002)PASCUAL, J. A. et al. Persistence of immobilised and total urease and phosphatase activities in a soil amended with organic wastes. Bioresource Technology, v. 82, n. 1, p. 73-78, 2002. observed that at 360 days after making an organic amendment in orchard soils, the increase in the urease activity persisted. In this same line, the ecological succession, both the natural and the one that causes the fallow in the rotations, is positively correlated with the urease activity (García et al. 2010GARCÍA, F. et al. Soil microbial biomass and activity under different agricultural management systems in a semiarid Mediterranean agroecosystem.Soil and Tillage Research, v. 109, n. 2, p. 110-115, 2010.).

This investigation aimed at evaluating the impacts of ecological and conventional agricultural managements on the enzymatic activities of soils under coffee cultivation, and their relationship with the resilience scores, in relation to the climatic variability reported for these agroecosystems.

MATERIAL AND METHODS

The study was carried out in 2015 and the selected study sites were composed of six coffee agroecosystems, being three ecological and three conventional, in Anolaima (Cundinamarca, Colombia), located at 1,650 m above the sea level. The study area has slopes with an inclination that ranges between 75 % and 100 %. Its soils are of the Inceptisol type, whose central feature is the susceptibility to mass removal. These soils also present high contents of expansive clays that generate the cracking of the ground in dry periods (Córdoba & León 2013CÓRDOBA, C.; LEÓN, T. Resiliencia de sistemas agrícolas ecológicos y convencionales frente a la variabilidad climática en Anolaima (Cundinamarca Colombia). Agroecología, v. 8, n. 1, p. 21-32, 2013.). The coffee plantations of both agroecosystems were ten years old.

The ecological agroecosystem sites were Don José, El Laurel and Los Pantanos (Table 1). These sites are characterized by being self-sufficient, carrying out soil conservation practices such as not using herbicides, insecticides, fungicides or mineral synthetic fertilizers. In these sites, biodiversity is employed as a strategy to manage insects and disease-causing agents. They also use organic fertilizers, drainage ditches and permanent coverage (Córdoba & León 2013CÓRDOBA, C.; LEÓN, T. Resiliencia de sistemas agrícolas ecológicos y convencionales frente a la variabilidad climática en Anolaima (Cundinamarca Colombia). Agroecología, v. 8, n. 1, p. 21-32, 2013.).

Table 1
Basic information of the study sites with ecological or conventional coffe agroecosystems.

The conventional agroecosystem sites were El Turista, La Cajita and Don Arturo (Table 1). The agricultural practices in these areas are based on the use of synthetic insecticides, fungicides and herbicides, such as aldrines, calbaryl (sevin), manzate and glyphosate (Córdoba & León 2013CÓRDOBA, C.; LEÓN, T. Resiliencia de sistemas agrícolas ecológicos y convencionales frente a la variabilidad climática en Anolaima (Cundinamarca Colombia). Agroecología, v. 8, n. 1, p. 21-32, 2013.). According to these authors, some fungi-based formulations (Beauveria bassiana and Metarhizium anisopliae) are also employed. The farmers of these conventionally managed farms do not keep track of quantity, frequency or corrective actions, regarding the doses of agrochemicals applied. In this way, the application of fertilizers and pesticides is made based on suggestions given by agrochemical marketers and using trial and error. In this sense, these applications are not preceded by technical recommendations and/or soil fertility studies, hence the difficulty of specifying quantities and corrective measures applied in each area.

The sampling was carried out in the first 20 cm of the soil depth. Quadrants of 10 m x 10 m were established in each agroecosystem, collecting samples in zigzag in five different points. At each point, five subsamples were taken and mixed to obtain a homogeneous composite sample. In total, thirty composite samples were collected, five for each of the agroecosystems.

Samples were taken in two seasons: in the months of highest (May) and lowest (August) rainfall rate, reported by the Institute of Hydrology, Meteorology and Environmental Studies of Colombia (IDEAM by its abbreviation in Spanish). The samples were transported under refrigeration and stored at -20 ºC.

The following physical proprieties were determined as it follows (IGAC 2006INSTITUTO GEOGRÁFICO AGUSTIN CODAZZI (IGAC). Métodos analíticos del laboratorio de suelos. 6. ed. Bogotá: IGAC, 2006., Avellaneda-Torres et al. 2018AVELLANEDA-TORRES, L. M.; LEÓN SICARD, T. E.; TORRES ROJAS, E. Impact of potato cultivation and cattle farming on physicochemical parameters and enzymatic activities of neotropical high Andean Páramo ecosystem soils. Science of the Total Environment, v. 631-632, n. 1, p. 1600-1610, 2018.): soil moisture; plasticity index, according to the Atterberg limits (minimum moisture, in which the soil can be rolled forming non-fragmented rods of 3 mm in diameter, and the liquid limit, with the “casuela de Casagrande”); and bulk density by the wax immersion method. The chemical assessed proprieties were: pH; electrical conductivity by saturated soil paste extract; organic carbon by the Walkley-Black method; total nitrogen; interchangeable bases (Ca, K, Mg, Na) by extraction with ammonium acetate; effective cation exchange capacity by displacement of NH4; interchangeable acidity by KCl extraction; available P (Bray II); micronutrients (Cu, Fe, Mn, Zn) by extraction with DTPA; and boron by extraction with mono calcium phosphate (IGAC 2006INSTITUTO GEOGRÁFICO AGUSTIN CODAZZI (IGAC). Métodos analíticos del laboratorio de suelos. 6. ed. Bogotá: IGAC, 2006., Avellaneda-Torres 2018AVELLANEDA-TORRES, L. M.; LEÓN SICARD, T. E.; TORRES ROJAS, E. Impact of potato cultivation and cattle farming on physicochemical parameters and enzymatic activities of neotropical high Andean Páramo ecosystem soils. Science of the Total Environment, v. 631-632, n. 1, p. 1600-1610, 2018.).

The urease activity was according to Alef & Nannipieri (1995)ALEF, K.; NANNIPIERI, P. Methods in applied soil microbiology and biochemistry. London: Academic Press, 1995., modified by Avellaneda-Torres (2008)AVELLANEDA-TORRES, L. M. Actividades enzimáticas de suelos con y sin historia de uso agrícola y manejo convencional y de sus consorcios bacterianos. 2008. 208 f. Thesis (M.Sc. in Chemical Science) - Universidad Nacional de Colombia, Colombia, 2008., which is based on the colorimetric determination at 690 nm of the released ammonia, after incubation with a solution of urea for 2 h, at 37 ºC (Alef & Nannipieri 1995ALEF, K.; NANNIPIERI, P. Methods in applied soil microbiology and biochemistry. London: Academic Press, 1995.).

The protease activity was determined by using casein as substrate, after incubation for 2 h at 50 ºC and pH 8.1. In this method, the released amino acids react with the Folin-Ciocalteu reagent in alkaline solution to form a blue complex that is colorimetrically determined (700 nm) (Ladd & Butler 1972LADD, J.; BUTLER, J. Short-term assays of soil proteolytic enzyme activities using proteins and dipeptide derivatives as substrates. Soil Biology and Biochemistry, v. 4, n. 1, p. 19-30, 1972.).

The acid and alkaline phosphatase activities were quantified by determining the p-nitrophenol that was released after the incubation with p-nitrophenyl phosphate solution for 1 h at 37 ºC (Alef & Nannipieri 1995ALEF, K.; NANNIPIERI, P. Methods in applied soil microbiology and biochemistry. London: Academic Press, 1995.). The p-nitrophenol was photometrically determined at 400 nm (Tabatabai & Bremner 1969TABATABAI, M.; BREMNER, J. Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biology and Biochemistry, v. 1, n. 4, p. 301-307, 1969. and Eivazi & Tabatabai 1988EIVAZI, F.; TABATABAI, M. Glucosidases and galactosidases in soils. Soil Biology and Biochemistry, v. 20, n. 5, p. 601-606, 1988., modified by Avellaneda-Torres 2008AVELLANEDA-TORRES, L. M. Actividades enzimáticas de suelos con y sin historia de uso agrícola y manejo convencional y de sus consorcios bacterianos. 2008. 208 f. Thesis (M.Sc. in Chemical Science) - Universidad Nacional de Colombia, Colombia, 2008.).

The β-glucosidase activity was determined by quantifying the p-nitrophenol released after the incubation with p-nitrophenyl glucoside solution for 1 h, at 37 ºC. The p-nitrophenol was photometrically determined at 400 nm (Alef & Nannipieri 1995ALEF, K.; NANNIPIERI, P. Methods in applied soil microbiology and biochemistry. London: Academic Press, 1995., modified by Avellaneda-Torres 2008AVELLANEDA-TORRES, L. M. Actividades enzimáticas de suelos con y sin historia de uso agrícola y manejo convencional y de sus consorcios bacterianos. 2008. 208 f. Thesis (M.Sc. in Chemical Science) - Universidad Nacional de Colombia, Colombia, 2008.). The soil samples collected in order to determine their enzymatic activity were transported in the shortest time possible at 4 ºC, until storage at -20 ºC in the laboratory. The determination of the enzymatic activities was carried out from the previously stored wet soil. Enzymatic activities were expressed by g of dry soil, determined from the gravimetric humidity of the soils at the time of analysis.

The enzymatic activities were related to the resilience scores of the climate variability of the agroecosystems under study. These scores were obtained from previous reports generated by Córdoba & León (2013)CÓRDOBA, C.; LEÓN, T. Resiliencia de sistemas agrícolas ecológicos y convencionales frente a la variabilidad climática en Anolaima (Cundinamarca Colombia). Agroecología, v. 8, n. 1, p. 21-32, 2013., which indicated the biophysical and cultural characteristics that determine the resilience to the climate variability of the aforementioned agroecosystems. These authors carried out evaluations in a scale from 1 to 5, drawn from 62 guidelines: 4 of the physical type, 5 related to soils, 4 to soil management, 8 to water management, 9 of biological diversity, 13 of social aspects, 7 related to economic aspects, 6 to institutional aspects, 3 of political aspects and 3 of technological level.

The relationships among data of soil enzymatic activities and resilience scores of climatic variability associated to the assessed agroecosystems were determined by multivariate analysis tools.

Normality and homoscedasticity tests were applied by using the Shapiro Wilk and Barttlet tests, respectively. Additionally, an average-to-average comparison was performed, by using the Wilcoxon and t-Student tests. To establish the relationships among physicochemical proprieties, enzymatic activities and biophysical and cultural characteristics that determine resilience to the climatic variability, canonical ordinations based on principal coordinates analysis were used (Anderson & Willis 2003ANDERSON, M. J.; WILLIS, T. J. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology, v. 84, n. 2, p. 511-525, 2003.). For the analyses, the package Permanova for Primer v6 software was used (Clarke & Warwick 2001CLARKE, K. R.; WARWICK, R. M. Change in marine communities: an approach to statistical analysis and interpretation. 2. ed. Plymouth: Plymouth Marine Laboratory, 2001., Anderson et al. 2008ANDERSON, M. J.; GORLEY, R. N.; CLARKE, K. R. Permanova for Primer: guide to software and statistical methods. Plymouth: PRIMER-E Ltd, 2008.).

RESULTS AND DISCUSSION

There were statistically significant differences (p < 0.05) associated to the soil managements for the following physicochemical proprieties: percentage of organic carbon, content of nitrogen in the soil and available boron. The means for this variables were higher in the ecological management, if compared with the conventional one (Table 2).

Table 2
Soil physicochemical proprieties assessed in ecological and conventional coffee agroecosystems, with sampling in two growing seasons.

All agroecosystems showed percentages of organic carbon ​​above 5 %, which can be considered very high organic carbon soils. The higher organic carbon content in the ecological farms may be related to the adopted soil conservation practices, such as weed management, use of slurry, composting, soil cover and zero tillage. These practices bring benefits such as a lower carbon expenditure by respiration and a greater immobilization in biomass, as well as the superficial accumulation of organic matter, among others (Sánchez de Prager et al. 2012SÁNCHEZ DE PRAGER, M. et al. El suelo, su metabolismo, ciclaje de nutrientes y prácticas agroecológicas. Agroecología, v. 7, n. 1, p. 19-34, 2012.). In this regard, it has been reported that the no-tillage increases the soil organic carbon values. Different types of management, such as fertilization and the use of pesticides, may affect the carbon storage (Roldán et al. 2005ROLDÁN, A. et al. Changes in soil enzyme activity, fertility, aggregation and C sequestration mediated by conservation tillage practices and water regime in a maize field. Applied Soil Ecology, v. 30, n. 1, p. 11-20, 2005.). This could explain the lower organic carbon content for the conventional sites (Ernani et al. 2001ERNANI, P.; RIBEIRO, M.; BAYER, C. Modificações químicas em solos ácidos ocasionadas pelo método de aplicação de corretivos da acidez e de gesso agrícola. Scientia Agricola, v. 58, n. 4, p. 825-831, 2001.).

The soil organic carbon content did not change with the sampling periods (Table 2), probably because the biodiversity in these agroecosystems becomes important facing adverse effects of climate variations, making them more resilient to this changes (Varela 2010VARELA, M. Evaluación de sistemas de producción agroecológicos incorporando indicadores de sostenibilidad en la sabana de Bogotá. 2010. 68 f. Thesis (M.Sc in Environrment and Development) - Universidad Nacional de Colombia, Bogotá, 2010.).

The content of nitrogen (N) differed statistically between the management systems, being also higher in the ecologically managed sites (Table 2). It was found that, in general, the means of this variable for the six sites were greater than 0.3 % of N, what places them as having a very high N content. The greater N content in the soil of the ecological agrosystem is consistent with the organic carbon content for the same agroecosystem. Furthermore, the lower N content in conventional sites may be related to practices such as the application of agrochemicals, which exerts a selective pressure on microorganisms, which, over time, can modify the physicochemical and biological characteristics of the soil (Manna & Singh 2001MANNA, M.; SINGH, M. Long-term effects of intercropping and bio-litter recycling on soil biological activity and fertility status of sub-tropical soils. Bioresource Technology, v. 76, n. 2, p. 143-150, 2001.). Environmental factors such as the content of organic matter and the availability of energy sources and other nutrients, as well as the presence of growth factors such as moisture, temperature, pH, redox potential and soil structure, may affect the ecology, activity and dynamics of the soil microbial community (Nannipieri et al. 2003NANNIPIERI, P. et al. Microbial diversity and soil functions. European Journal of Soil Science, v. 54, n. 4, p. 655-670, 2003.).

The urease activity was statistically higher in the soil under ecological management, if compared with the conventional one (Table 3). This would indicate that the conventional management practices are decreasing the activity of urease, corroborating Dick et al. (1988)DICK, R.; RASMUSSEN, P.; KERLE, E. Influence of long-term residue management on soil enzyme activities in relation to soil chemical properties of a wheat-fallow system. Biology and Fertility of Soils, v. 6, n. 2, p. 159-164, 1988., who showed that the urease and amidase activities decreased with the increasing application of ammonia-based fertilizers in a conventional soil management. The addition of the final product of the enzymatic reaction (NH4+) decreased the activity of the enzymes (Bandick & Dick 1999BANDICK, A. K.; DICK, R. P. Field management effects on soil enzyme activities. Soil Biology and Biochemistry, v. 31, n. 11, p. 1471-1479, 1999.).

Table 3
Enzymatic activities of soils under ecological and conventional coffee agroecosystems with sampling in two growing seasons.

The increased activity of urease under ecological management may be due to soil conservation practices, such as the use of organic fertilizers and permanent coverage, that result in a better functioning of the nitrogen cycle in the soil. These results have been observed when conservation tillage and conventional tillage are compared, confirming that tillage practices allow for a greater activity of urease throughout the crop cycle, due to the content of organic matter that favors the maintenance of this activity in the soil (Contreras et al. 2005CONTRERAS, F.; PAOLINI, J.; RIVERO, C. Efecto de la adición de enmiendas orgánicas sobre las actividades enzimáticas (deshidrogenasa, ureasa, fosfomonoesterasa ácida y arilsulfatasa) y la mineralización del carbono en suelos del municipio Rivas Dávila (estado Mérida). Venesuelos, v. 10, n. 1, p. 12-17, 2005.).

Statistically significant differences were also found in the urease activity between sampling seasons (Table 3), being higher in the dry season, when compared with the rainy season. This may be related to the influence of water content, temperature, pH and buffer capacity, cation exchange capacity and nitrogen compounds (Salamanca 2008SALAMANCA, C. Efecto de las fuentes orgánicas obtenidas de los subproductos agroindustriales de la caña de azúcar (Saccharum officinarum L.) y el plátano (Musa spp.) sobre la actividad microbiana y enzimático en el suelo. 2008. 63 f. Thesis (M.Sc in Agricultural Sciences) - Universidad Nacional de Colombia, Palmira, 2008.).

The protease activity did not show statistically significant differences between the management systems (Table 3). The same result can be observed regarding the effect of the climate condition at the sampling seasons on the protease activity.

The acid and alkaline phosphatase activities showed statistically significant differences between the management systems, being greater under the ecological management, if compared with the conventional one (Table 3). These results coincide with those reported by Oberson et al. (1996)OBERSON, A. et al. Microbiological processes in soil organic phosphorus transformations in conventional and biological cropping systems. Biology and Fertility of Soils, v. 21, n. 3, p. 138-148, 1996., who found that the activity of the acid phosphatases was higher in soils under ecological and biodynamic cultivation than in the conventionally managed ones. They argued that the incorporation of organic matter into the soil increases the mineralization of organic phosphorus, thus promoting the P biogeochemical cycle. They also observed that the activity of acid phosphatase was higher in soils covered in prairie with high organic matter contents, both in the rainy and dry seasons. In addition, the acid phosphatase activity is stimulated by the soil microbial activity, amount of substrates that are available, soil moisture (Gálviz et al. 2007GÁLVIZ, C.; BURBANO, H.; BONILLA, C. Actividad de fosfatasa ácida en suelos cultivados con papa y praderas del corregimiento de Catambuco, Pasto - Colombia. Acta Agronómica, v. 56, n. 1, p. 13-16, 2007.), crops, management practices and production systems. The positive impact of the organic production on alkaline phosphatase (compared to the conventional production), or the application of organic products in the fertilization of crops, has also been demonstrated by Quenum (2010)QUENUM, L. Comparación entre la producción ecológica e integrada de hortalizas en base a parámetros del cultivo y del suelo. 2010. 289 f. Thesis (Ph.D in Vegetal Production) - Universidad Politécnica de Valencia, Valencia, 2010..

The lower activity of phosphatases under conventional systems could be related to the higher availability of phosphorous. Considering that enzymatic activities, especially phosphatases, are inhibited when exposed to a high availability of labile P, the fertilization practices, especially with P fertilizers, could suppress the secretion of enzymes involved in the mineralization of organic P in the long term (Zamora et al. 2005ZAMORA, F.; MOGOLLÓN, J.; RODRÍGUEZ, N. Cambios en la biomasa microbiana y la actividad enzimática inducidos por la rotación de cultivos en un suelo bajo producción de hortalizas en el estado Falcón, Venezuela. Multiciencias, v. 5, n. 1, p. 62-70, 2005.).

Acid and alkaline phosphatases also showed statistically significant differences between seasons (Table 3), generating a greater activity of this enzyme in the dry season, if compared with the rainy one. This indicates that, with a decrease in the rainfall, the ecological management favors the biogeochemical cycle of phosphorus. A similar study by Yoshioka et al. (2006)YOSHIOKA, I.; SÁNCHEZ DE PRAGER, M.; BOLAÑOS, M. Actividad de fosfatasas ácida y alcalina en suelo cultivado con plátano en tres sistemas de manejo. Acta Agronómica, v. 55, n. 1, p. 1-8, 2006. differs from the results obtained, reporting a greater activity of the alkaline phosphatase in the conventional management, and a lower one for the traditional and organic managements. This was associated with the greater activity of microorganisms as an energy expenditure, since the behavior of this enzyme is related to the activity of soil bacteria and fungi (Criquet et al. 2004CRIQUET, S. et al. Annual dynamics of phosphatase activities in an evergreen oak litter: influence of biotic and abiotic factors. Soil Biology and Biochemistry, v. 36, n. 1, p. 1111-1118, 2004., Dick 1997DICK, R. P. Soil enzyme activities as integrative indicators of soil health. In: PANKHURST, C. E.; DOUBE, B. M.; GUPTA, V. V. S. R. (Eds.). Biological indicators of soil health. Wellingford: Cabi, 1997. p. 121-156.), what leads to an accelerated metabolism that is reflected in the enzymatic activity (Sánchez de Prager 2003SÁNCHEZ DE PRAGER, M. Actividad biológica en la rizósfera del maracuyá (Pasiflora edulis var. Flavicarpa) en diferentes sistemas de manejo, estados de desarrollo y condiciones fitosanitarias. 2003. 261 f. Thesis (Ph.D in Agricultural Engineering) - Universidad Politécnica de Madrid, Madrid, 2003.). A higher rate of residues input brings with it a greater development of microorganisms and, therefore, a higher production of enzymes (Bandick & Dick 1999BANDICK, A. K.; DICK, R. P. Field management effects on soil enzyme activities. Soil Biology and Biochemistry, v. 31, n. 11, p. 1471-1479, 1999.).

Similarly to the urease and phosphatases, the ß-glucosidase activity was statistically higher in the soils under ecological management, when compared with the conventional one (Table 3). This may be due to the fact that the enzymatic activities and microorganisms that secrete them are sensitive to the application of herbicides (Alvear et al. 2006ALVEAR, M. et al. Efecto de la aplicación de herbicidas en condiciones de campo sobre algunas actividades biológicas. Revista Ciencia del Suelo y Nutricón Vegetal, v. 6, n. 1, p. 64-76, 2006.), and that the microorganisms reduce the enzyme production rate under excess of inorganic fertilizers (González-Prieto & Carballas 1995GONZÁLEZ-PRIETO, S.; CARBALLAS, T. N biochemical diversity as a factor of soil diversity. Soil Biology and Biochemistry, v. 27, n. 2, p. 205-210, 1995.). These results are similar to those reported by Ochoa et al. (2007)OCHOA, V. et al. Actividades enzimáticas como indicadores de calidad del suelo en agroecosistemas ecológicos. Iniciación a la Investigación, v. 2, n. 1, p. 1-10, 2007., who found a greater activity of dehydrogenase, β-glucosidase and arylsulfatase in the soil where there was a minimal tillage, if compared with the conventional tillage.

The activity of ß-glucosidase, however, was not statistically influenced by the growing seasons. This may be due to the fact that, in these agroecosystems, in general, peasant practices are used, such as polycrop and cover; therefore, the mulching of the soil surface reduces temperature oscillations, keeping it cool, maintaining the soil moisture during hot and dry seasons and promoting a microbial activity and crop development (Albiach et al. 2006ALBIACH, R. et al. Sobre las enzimas del suelo y sus técnicas de medida. Edafología, v. 13, n. 3, p. 117-125, 2006.).

Figure 1 shows an important grouping, in relation to the management systems, confirming the results from the univariate analysis (Table 3). Thus, the use of organic inputs and permanent coverage are benefiting the activity of the hydrolytic enzymes and favoring the recycling of carbon and nutrients in these soils.

Figure 1
Canonical analysis of the principal coordinates, based on enzymatic activities and physicochemical proprieties of soils, under ecological (organic) or conventional management, in two growing seasons of the coffee agroecosystems.

The agricultural management influences the soil microorganisms and microbial processes due to changes in the quantity and quality of plant residues that enter the soil, their spatial distribution, changes in the supply of nutrients and physical changes (Christensen 1996CHRISTENSEN, B. T. Matching measurable soil organic matter fractions with conceptual pools in simulation models of carbon turnover: revision of model structure. In: POWLSON, D. S.; SMITH, P. et al. (Eds.). Evaluation of soil organic matter models using existing long-term datasets: global environmental change. Berlin: Springer, 1996. p. 143-160.). On the other hand, conventional agroecosystems, in general, tend to contrast with ecological agroecosystems. Conventional management practices, such as the use of pesticides, herbicides and synthetic fertilizers, are inhibiting the enzymatic activities in the aforementioned agroecosystems; and such indicators of soil quality may help to predict early changes caused by agricultural practices. As some researchers indicate, agrochemicals can produce negative environmental impacts on ecosystems (Norgaard & Sikor 1995NORGAARD, R.; SIKOR, T. Metodología y práctica de la agroecología. In: ALTIERI, M. (Ed.). Agroecología: bases científicas para una agricultura sustentable. Montevideo: Clades, 1995. p. 27-42.). Conventional agriculture causes the reduction of soil fertility and compaction and a decrease of the organic matter and the biodiversity associated with it, such as microorganisms responsible for the production of soil enzymes (Rosset 1997ROSSET, P. La crisis de la agricultura convencional, la sustitución de insumos y el enfoque agroecológico. Revista de Agroecología y Desarrollo, v. 11/12, n. 1, p. 2-12, 1997.).

Enzymatic activities of the ecological agroecosystems are related to higher levels of magnesium, pH, boron, zinc and phosphorus, indicating that these soil characteristics favor enzymatic activities in those sites; while the conventional agroecosystems are correlated with iron, interchangeable acidity and manganese (Figure 1).

The sampling period was another important grouping criterion, since there was a trend for clustering in the dry season, in agreement with the univariate analysis (Table 3), which showed statistically significantly higher enzymatic activities in the drought. Thus, the biochemical indicators are sensitive to climate variability, and are favored by low rainfall and high temperatures.

The enzymatic activities of ecological management are correlated with the variables that refer to the non-purchase of inputs, what means that the fact of not acquiring or relying on these external inputs gave them a high score, in terms of resilience (Figure 2). Likewise, variables such as the non-use of pesticides and herbicides, non-dependence on pesticides and use of external fertilizers, which are also correlated with the enzymatic activities of the ecological management, suggest that the non-use of chemical synthesis products improves the resilience scores of the agroecosystems and favors their soil enzymatic activities.

Figure 2
Canonical analysis of the principal coordinates based on soil enzymatic activities and resilience scores of agroecosystems, under ecological and conventional management, in two growing seasons of coffee plantations.

The enzymatic activities of the ecological agroecosystems were related to the fact that the respective farmers belong to some type of organization, what may be positively influencing other variables that increase its resilience scores, such as the use of soil conservation practices, weed management, farmers' knowledge about pollination, microorganisms in general and nitrogen-fixing microorganisms, which are closely related to the high content of nitrogenous substrates and the origin of organic material. Similarly, the low presence of pests in these agroecosystems is due to the fact that farmers use the biodiversity as a management strategy for insects and disease agents, which favors high enzymatic activities and resilience scores of the ecosystem.

The enzymatic activities of the conventional agroecosystems showed a relation with the variables savings and extra income, since the respective peasants may have higher incomes from their crops, if compared to those normally obtained from the ecological ones. The relation of the ecological agroecosystems with a higher percentage of workers that have been hired in these sites may be linked to the need for fertilization and soil tillage.

CONCLUSIONS

  1. The enzymatic activities are modified by the management systems, and these are specifically favored by the ecological management. Hence, in the long term, this agroecosystem ensures an efficient use of the soil resources with a lower degradation and contamination;

  2. Urease, acid and alkaline phosphatase activities are sensitive to climate variability, and are favored by low rainfall and high temperatures;

  3. The resilience scores to climate variability that showed the highest correlations with the enzymatic activities and with the ecological agroecosystems were the farmers' knowledge of soil microorganisms, non-use of pesticides and synthetic fertilizers, non-dependence on external inputs, use of soil conservation practices and belonging to some peasant organization.

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Publication Dates

  • Publication in this collection
    Oct-Dec 2018

History

  • Received
    10 Apr 2018
  • Accepted
    22 May 2018
  • Published
    30 Nov 2018
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