Revista Cubana de Ciencias Forestales. May-August, 2019, 7(2): 171-183
Translated from the original in spanish
Evaluation of biological and biochemical parameters in a soil under different forest species of the Argentinian Patagonia
Evaluación de parámetros biológicos y bioquímicos en un suelo bajo distintas especies forestales de la Patagonia Argentina
Gabriela Cristina Sarti1
Diana N. Effrona1
1Universidad de Buenos Aires, Argentina. Facultad de Agronomía. Argentina. E-mail: karibu@agro.uba.ar
Received: January 18th, 2019.
Approved: May 3rd , 2019.
ABSTRACT
In forest systems, the decomposition of litterfall is the main route of entry of nutrients into the soil and is one of the key points of recycling organic matter and nutrients. The rate at which all plant debris decomposes depends on environmental factors and the material provided by different forest species. The objective of this work was to evaluate the effect of vegetation cover on biological and biochemical parameters in a soil beneath two native forest species of the Mountain range (Austrocedrus chilensis (Don) Flor. et Boutl.), radal (Lomatia hirsuta Diels.), an exotic European Oak (Quercus robur) and an area adjacent to the forest that has only shrub vegetation. The activity of the enzymes ß-glucosidase, phosphatase, protease and microorganism counts were studied. In the leaf litter of each forest species, the levels of N, P, lignin and cellulose were measured. The results showed that the biological activity was higher in the soil under the forest species than in the area adjacent to the forest. At the same time, the litterfall corresponding to the European oak, presented the lowest contents of recalcitrant substances such as lignin and cellulose and the highest contents of N and P, this would facilitate the activity of soil microorganisms facilitating the decomposition of plant material. It was concluded that from the microbiological point of view the implantation of the species Roble would propitiate a better quality of the forest soil.
Keywords: enzymatic activities; cypress of mountain range; radal; european oak.
RESUMEN
En los sistemas forestales, la descomposición de la hojarasca es la principal vía de entrada de los nutrientes en el suelo y es uno de los puntos clave del reciclado de la materia orgánica y nutrientes. La tasa a la cual se descomponen todos los restos vegetales depende de factores ambientales y del material aportado por las distintas especies forestales. El objetivo de este trabajo fue evaluarel efecto de la cubierta vegetal sobre parámetros biológicos y bioquímicos en un suelo debajo de dos especies forestales nativas ciprés de la Cordillera (Austrocedrus chilensis (Don) Flor. et Boutl.), radal (Lomatia hirsuta Diels.), una especie exótica Roble europeo (Quercus robur) y un área adyacente al bosque que posee sólo vegetación arbustiva. Se estudió la actividad de las enzimas ß-glucosidasa, fosfatasa, proteasa y recuentos de microorganismos. En la hojarasca de cada especie forestal, se midieron los niveles de N, P, lignina y celulosa. Los resultados mostraron que la actividad biológica fue mayor en el suelo bajo las especies forestales que en el área adyacente al bosque. A su vez, la hojarasca que corresponde al roble europeo, presentó los menores contenidos de sustancias recalcitrantes como lignina y celulosa y los mayores contenidos de N y P, esto facilitaría la actividad de los microorganismos del suelo facilitando la descomposición del material vegetal. Se concluyó que desde el punto de vista microbiológico la implantación de la especie Roble propiciaría una mejor calidad del suelo forestal.
Palabras clave: actividades enzimáticas; ciprés de la cordillera; radal; roble europeo.
INTRODUCTION
Forests are important ecosystems for mitigating the effects of climate change because of their ability to store carbon in their biomass. They provide essential habitat for a wide range of species of flora and fauna, minimize soil degradation and contribute to maintaining water, nutrient and energy cycles.
The production and speed of decomposition of organic waste provided by the canopy of the forest conditions the thickness of litter accumulated on the ground, being the leaves the majority fraction of this material. In forest systems, the decomposition of litterfall is the main route of entry of nutrients into the soil and is one of the key points for recycling organic matter and nutrients (Molina et al., 2018). This litterfall consists of a wide range of compounds that are classified into six main groups:
a) cellulose,
b) hemicellulose,
c) lignin,
d) water-soluble fraction (amino acids, simple sugars, aliphatic acids),
f)
alcohol-soluble constituents (fats, oils, waxes, resins),
e) proteins.
Polysaccharides are the most abundant carbohydrates, usually dominating hexoses over pentoses (Beltrán et al., 2017). All fractions are gradually incorporated into the soil ensuring the permanent contribution of nutrients to the soil. On the other hand, these different types of vegetation cover affect the physical, chemical, biological and biochemical properties of soils (Capulin et al., 2018).
The rate at which all plant remains decompose depends on environmental factors such as temperature, rainfall and also depends on different forest species (Moreno Valdez et al., 2018). Therefore, in order to evaluate the quality of a soil it is necessary to have physical, chemical and biological indicators that will differ according to the type of soil, vegetation cover, climate, time of sampling and use. For this reason, it is necessary to have reference values for each type of soil. Before the use of the concept of soil quality, only physical and chemical parameters were used as indicators.
Biological parameters such as enzymatic activities are considered sensitive and early indicators of soil changes to disturbances and can then be used to predict long-term trends in soil quality (Burns et al., 2013). Much of the enzymatic activity comes from the mass of microorganisms present in the soil. These microorganisms play a fundamental role in the sustainability of diverse ecosystems by developing essential functions such as cycling nutrients for plant growth, formation of soil humus, improvement of physical properties and maintenance of ecosystem biodiversity. Several studies maintain that the composition of the soil microbial community can be influenced by the plant species present (Quintero et al., 2014). On the other hand, the variations of the microbial population are temporary, depending on the availability of the most labile substrates (Kätterer et al., 2014).
The objective of this work is to study the effect of vegetation cover on biological and biochemical parameters in a soil beneath two forest species native to the mountain range (Austrocedrus chilensis (Don) Flor. et Boutl.), radal (Lomatia hirsuta Diels.), an exotic European oak species (Quercus robur) and an area adjacent to the forest that has only shrub vegetation.
MATERIALS AND METHODS
Study site
The area under study is located at INTA Forest Station in Trevelín, Chubut, Argentina Lat. 43º South, Longitude 71º 31' West, altitude 470 m. s. n. m. The surface area of the station is 3,020 ha. The soil corresponds to an Andisol. The original material is composed of volcanic ash mixed with colluvial material. The climate is characterized by average annual rainfall of 942 mm, producing 80.6% of them between the months of April and September. The maximum annual average temperature is 15.7 ºC and the minimum annual average is 3.4 ºC. In the season, there are extensive areas of native forest and numerous experimental plots implanted with various species. The soils of the forest station are classified as Andisoles, which through the meteorization of the parental material develop non-crystalline structures and Al-Humus complexes that define their properties, among them are distinguished variable load, high capacity of fixation of phosphorus, low apparent density and formation of stable aggregates (Dörner et al., 2009).
At the study site, a native forest area was selected where the main forest species are Cordillera Cypress (Austrocedrus chilensis (Don) Flor. et Boutl.) and Radal (Lomatia hirsuta Diels.) and the rest of the present vegetation is composed of the species: Laura (Schinus patagonicus), Vinagrillo (Rumex acetocella), maitén (Maytenus boaria), rosehip (Rosa eglanteria), Indian tobacco (Verbascum thapsus), Patagonian barley (Bromus patagonicus) and fescue (Festuca arundinacea) and an area of forest implanted with the 50-year-old European oak forest species (Quercus robur).
Ten trees were randomly selected from each of the species of similar size with good health status. The samples were collected in October 2017. Surface samples (0-10cm) were taken after clearing the surface plant material and at the same distance from the trunk of the selected trees. Under each of the trees, four samples were taken from which a composite tree sample was taken on which analytical determinations were made. The wet samples were stored in plastic bags that were kept refrigerated until their analysis in the laboratory. The samples were sieved by a mesh of 4 mm or 2 mm depending on the determination to be made. The results were expressed on the basis of air-dried soil to constant weight.
Analytical determinations on soil samples
The following determinations were made on the ten composite samples taken under each species and in the area adjacent to the forest, the analyses were carried out in duplicate.
The extracellular enzymatic activities involved in the C (ß-glucosidase), N (proteases) and P (acid phosphatase) cycles were determined. In the cases of ß-glucosidase and phosphatase, enzyme activity was measured by incubating the sample with a specific substrate (p-nitrophenyl glycoside and p-nitrophenyl sodium phosphate respectively) and subsequent colorimetric determination of the p-nitrophenol formed. Protease activity was determined by incubating the soil with casein and subsequent colorimetric determination of the released tyrosine.
The following determinations were done on four of the ten composite samples taken under each species and the analyses were performed in duplicate.
Recounting of total bacteria, amylolytics, actinomycetes and total fungi: suspensions and appropriate soil dilutions were made to do the counts in solid culture media.
Analytical determinations on vegetable material
Determination of total nitrogen:
An acid digestion was made with concentrated sulphuric acid and a mixture of ferrous sulphate and copper sulphate. The organic nitrogen was converted to ammonium sulphate, the solution was alkalinized and the released ammonium was titled with a sulphuric acid solution. The results were expressed in g of N Kg.-1 dry matter.
Determination of total phosphorus
The present phosphorus was extracted with 0,1N HCl and NH4 F 0,03N HCl extraction solution. Subsequently, it was agitated, filtered and on an aliquot of the filtrate a mixture of a solution of ammonium molybdate and ascorbic acid was added, obtaining a coloured product that was read at 660 nm. The results were expressed in g P kg.-1 dry matter.
Determination of lignin and cellulose
The acid-detergent fibre method was used. On 1g of the ground sample an acid hydrolysis was carried out using ethyltrimethylammonium bromide as detergent and sulphuric acid for 1 hour. The faculty of ethyltrimethylammonium bromide was used to denature proteins. The obtained material was dried at 110 ºC and weighed. The result was calculated as a percentage of the starting material. The fiber is composed of cellulose and lignin and these materials can be measured separately. The results were expressed in g lignin 100 g-1 dry matter and g cellulose 100 g-1 dry matter.
Statistical analysis
Statistical analysis for the variables ß-glucosidase, acid phosphatase and protease was done with Infostat software version 1.8, the normal distribution of the data was analyzed with the Levene test and the homogeneity of variances by Shapiro-Wilkins test the data were analyzed statistically by a one-way variance analysis corresponding to a completely randomized design.
Differences between treatment means were determined by Tukey's test (p<0.05).
RESULTS AND DISCUSSIONS
The enzymes involved in the carbon, phosphorus and nitrogen cycles such as â-glucosidase, acid phosphatase and protease showed significant differences between the activities of these enzymes in the soil under the forest species studied and the area adjacent to the forest, being in all cases greater (p<0.05) the activity in the soil under the influence of forest species.
When comparing between forest species, the European Oak species showed the highest values of activity ß-glucosidase and acid phosphatase being the same 600 mg p-nitrophenol g-1 soil and 900 g p-nitrophenol g-1 soil respectively. In the case of protease activity, no significant differences were observed between the forest species studied (Figure 1, Figure 2, Figure 3).
Fig. 1. - Mean values of ß-glucosidase activity measured in the soil under the forest species under study and the adjacent soil
Different letters for each variable measured in the soil indicate significant differences (P <0.05).
Fig. 2. - Mean values of acid phosphatase activity measured in the soil under the forest species under study and the adjacent soil
Different letters for each variable measured in the soil indicate significant differences (P <0.05).
Fig. 3. - Average values of protease activity measured in the soil under the forest species under study and the adjacent soil
Different letters for each variable measured in the soil indicate significant differences (P <0.05).
Taking into account the forest species studied, recounts of total bacterial flora, fungi and actinomycetes were higher in the soil under the oak species. In the case of total bacterial flora and actinomycetes the recounts under oak were significantly higher than for the other species. For all the variables studied, the lowest recounts were obtained in the soil adjacent to the forestations (Table 1).
Table 1. - Recounts of fungi, bacteria and actinomyces measured in the soil under the cypress forest species of the mountain range
(Austrocedrus chilensis (Don) Flor. et Boutl.), radal (Lomatia hirsuta Diels.) and European oak (Quercus robur) and adjacent soil.
Table #2 shows the contents of recalcitrant substances such as lignin and cellulose as well as the contents of N and P foliar contributed by each forest species and the results show that the leaf litter corresponding to the oak species has the lowest content of recalcitrant substances as well as the highest values of N and P foliar (Table 2).
Table 2. - Values of lignin, cellulose, N and P in senescent leaves of the forest species in study cypress of the mountain range
(Austrocedrus chilensis (Don) Flor. et Boutl.), radal (Lomatia hirsuta Diels.) and European oak (Quercus robur).
Different letters for each variable measured in the soil indicate significant differences (P<0.05)
Taking into account the count of each of the types of microorganisms under study, the most contrasting results were found in the soil under forest species and the soil adjacent to the forest, with the highest values being found for all variables studied in the soil under forest species (Table 1). Villegas (2004) when comparing the soil of a pine forest (Pinus patula) and a soil with agricultural crops (rich in organic matter), found that the development of the bacterial population is lower in the case of the pine forest, this is attributed to the fact that the layer of leaves that accumulates under the conifer (Pinus patula) inhibits the development of some microorganisms for root-soil interaction. However, the work presented by Li, (2015) suggests that the highest rate of enzymatic activity is found in pine forests.
In the case of the forest species studied, recounts of total bacterial flora, fungi and actinomycetes are higher in the soil under the oak species (Table 1).
This could be explained by taking into account the different composition of the vegetal material contributed by each of the forest species. The data shown in Table 2, which positions European oak as the species that provides a litterfall with the highest contents of N and P and the lowest contents of recalcitrant substances, would imply that its residues have a simple chemical composition of easy degradation, this would favour the greater development of bacterial flora in the soil under this species. Defrieri et al., (2007) in a work with native species of a native forest of Chaco, Argentina, found for the case of the enzymatic activities protease and phosphatase significant differences in the use of different carbon sources according to the forest species under study. Similar results were found by Ushio et al., (2008), who found that the composition of the microbial community showed significant differences between coniferous and broadleaf species, attributing these differences to the effect that forest species have on soil properties such as pH, total C and N, which could be important factors influencing the composition of the soil microbial community.
The higher content of N and P in litterfall corresponding to the oak species (Table 2) strengthens the idea that these vegetal residues would be the most easily decomposable and suitable for the development of a prolific microbial activity especially in the case of bacteria and this is linked to the higher values found for ß-glucosidase activity and acid phosphatase in the soil under this forest species (Figure 1) and (Figure 2). However, there is no association between protein activity (Figure 3) and foliar N contributed by oak litter (Table 2), because there are no significant differences between enzyme activity in any of the forest species studied. Similar results linked to the lack of association between N levels and protease activity were found by Defrieri et al., (2010) in a forest andisol implanted with pine and ash.
In this work it is observed that the different leaves contributed by the forest species produce changes in the microbial communities, and in the levels of released extracellular enzymes. These results coincide with Alvear et al., (2007) who proposed that changes in the soil microorganism community depend on the origin and qualitative and quantitative composition of the organic matter present.
The results show the great dependence that exists between the biological parameters and the type of vegetal cover, finding the most contrasting situations when comparing the area adjacent to the forest and the soil under the influence of the forest species that contribute a greater content of vegetal residues of variable chemical composition.
The leaf litter corresponding to the oak species, due to its lower content of recalcitrant substances and the higher content of N and P, would facilitate the decomposition of vegetal material and this would be linked to the higher microbial counts and enzymatic activities for the soil under this species. It is concluded that the indicators studied showed a trend towards better soil quality from the microbiological point of view when under oak forest species.
BIBLIOGRAPHICAL REFERENCES
ALVEAR, M., REYES, F., MORALES, A., ARRIAGADA, C. y REYES, M., 2007. Actividad biológica y agregados estables al agua en dos tipos de formaciones vegetales de un bosque templado del Centro-Sur de Chile con perturbación antrópica. Ecología austral [en línea], vol. 17, no. 1, pp. 113-122. [Consulta: 27 febrero 2019]. ISSN 1667-782X. Disponible en: http://www.scielo.org.ar/scielo.php?script=sci_abstract&pid=S1667-782X2007000100010&lng=es&nrm=iso&tlng=es.
BELTRÁN PINEDA, M.E., ROCHA GIL, Z.E., BERNAL FIGUEROA, A.A. y PITA MORALES, L.A., 2017. Microorganismos funcionales en suelos con y sin revegetalización en el municipio de Villa de Leyva, Boyacá. Revista Colombia Forestal [en línea], vol. 20, no. 2. [Consulta: 23 abril 2019]. DOI https://doi.org/10.14483/udistrital.jour.colomb.for.2017.2.a05. Disponible en: https://revistas.udistrital.edu.co/ojs/index.php/colfor/article/view/10400.
BURNS, R.G., DEFOREST, J.L., MARXSEN, J., SINSABAUGH, R.L., STROMBERGER, M.E., WALLENSTEIN, M.D., WEINTRAUB, M.N. y ZOPPINI, A., 2013. Soil enzymes in a changing environment: Current knowledge and future directions. Soil Biology and Biochemistry [en línea], vol. 58, pp. 216-234. [Consulta: 27 febrero 2019]. ISSN 0038-0717. DOI 10.1016/j.soilbio.2012.11.009. Disponible en: http://www.sciencedirect.com/science/article/pii/S0038071712004476.
CAPULIN-GRANDE, J., SUÁREZ-ISLAS, A., RODRÍGUEZ-LAGUNA, R., MATEO-SÁNCHEZ, J.J., RAZO-ZÁRATE, R. y ISLAS-SANTILLÁN, M., 2018. Influence of fire on soil and vegetation properties in two contrasting forest sites in Central México. Ciencia e investigación agraria [en línea], vol. 45, no. 2, pp. 128-137. [Consulta: 27 febrero 2019]. ISSN 0718-1620. DOI 10.7764/rcia.v45i2.1798. Disponible en: https://scielo.conicyt.cl/scielo.php?script=sci_abstract&pid=S0718-16202018000200128&lng=es&nrm=iso&tlng=en.
DEFRIERI, R.L., EFFRON, D., PRAUSE, J., TORTAROLO, F., SARTI, G. y JIMÉNEZ, M.P., 2007. Ecosistema forestal nativo: influencia de las especies forestales sobre algunas propiedades microbiológicas en un monte chaqueño argentino. En: E. BEDMAR, C. OLMEDO, A. THUAR y E. CASTRO (eds.), Biología de Suelos. Argentina: Río Cuarto, ISBN 978-950- 665-438-2.
DEFRIERI, R.L., SARTI, G., TORTAROLO, M.F. y EFFRON, D., 2010. Propiedades bioquímicas y microbiológicas en un suelo de la Patagonia argentina con especies forestales implantadas. XXII Congreso Argentino de Ciencia del Suelo. Rosario, Argentina: Congreso Argentino de Ciencia del Suelo, ISBN 978-987-24771-1-0.
DÖRNER, J., DEC, D., PENG, X. y HORN, R., 2009. EFECTO DEL CAMBIO DE USO EN LA ESTABILIDAD DE LA ESTRUCTURA Y LA FUNCIÓN DE LOS POROS DE UN ANDISOL (TYPIC HAPLUDAND) DEL SUR DE CHILE. Revista de la ciencia del suelo y nutrición vegetal [en línea], vol. 9, no. 3, pp. 190-209. [Consulta: 23 abril 2019]. ISSN 0718-2791. DOI 10.4067/S0718-27912009000300003. Disponible en: https://scielo.conicyt.cl/scielo.php?script=sci_abstract&pid=S0718-27912009000300003&lng=es&nrm=iso&tlng=es.
KÄTTERER, T., BÖRJESSON, G. y KIRCHMANN, H., 2014. Changes in organic carbon in topsoil and subsoil and microbial community composition caused by repeated additions of organic amendments and N fertilisation in a long-term field experiment in Sweden. Agriculture, Ecosystems & Environment [en línea], vol. 189, pp. 110-118. [Consulta: 27 febrero 2019]. ISSN 0167-8809. DOI 10.1016/j.agee.2014.03.025. Disponible en: http://www.sciencedirect.com/science/article/pii/S0167880914001613.
LI, J., COOPER, J.M., LIN, Z., LI, Y., YANG, X. y ZHAO, B., 2015. Soil microbial community structure and function are significantly affected by long-term organic and mineral fertilization regimes in the North China Plain. Applied Soil Ecology [en línea], vol. 96, pp. 75-87. [Consulta: 27 febrero 2019]. ISSN 0929-1393. DOI 10.1016/j.apsoil.2015.07.001. Disponible en: http://www.sciencedirect.com/science/article/pii/S0929139315300378.
MOLINA, N.F., BARRIOS, J.R. y LEON, S.I., 2018. Caída y descomposición de hojarasca en los bosques ribereños del manantial de Cañaverales, Guajira, Colombia. Acta Biológica Colombiana [en línea], vol. 23, no. 1, pp. 115-123. [Consulta: 23 abril 2019]. ISSN 1900-1649. DOI 10.15446/abc.v23n1.62342. Disponible en: https://revistas.unal.edu.co/index.php/actabiol/article/view/62342.
MORENO VALDEZ, M.E., DOMÍNGUEZ GÓMEZ, T.G., ALVARADO, M. del S., COLÍN, J.G., CORRAL RIVAS, S. y GONZÁLEZ RODRÍGUEZ, H., 2018. Aporte y descomposición de hojarasca en bosques templados de la región de El Salto, Durango. Revista mexicana de ciencias forestales [en línea], vol. 9, no. 47, pp. 70-93. [Consulta: 23 abril 2019]. ISSN 2007-1132. DOI 10.29298/rmcf.v9i47.180. Disponible en: http://www.scielo.org.mx/scielo.php?script=sci_abstract&pid=S2007-11322018000300070&lng=en&nrm=iso&tlng=es.
QUINTERO, A.C., BARLIZA, J.C., PELÁEZ, J.D.L. y TURIZO, C.E.T., 2014. Caracterización de materia orgánica aportada por hojarasca fina en los bosques de ribera del río Gaira (Sierra Nevada de Santa Marta Colombia). RIAA [en línea], vol. 5, no. 1, pp. 171-184. [Consulta: 27 febrero 2019]. ISSN 2145-6453. Disponible en: https://dialnet.unirioja.es/servlet/articulo?codigo=5344959.
USHIO, M., WAGAI, R., BALSER, T.C. y KITAYAMA, K., 2008. Variations in the soil microbial community composition of a tropical montane forest ecosystem: Does tree species matter? Soil Biology and Biochemistry [en línea], vol. 40, no. 10, pp. 2699-2702. [Consulta: 27 febrero 2019]. ISSN 0038-0717. DOI 10.1016/j.soilbio.2008.06.023. Disponible en: http://www.sciencedirect.com/science/article/pii/S0038071708002241.
VILLEGAS, J.C., 2004. ANÁLISIS DEL CONOCIMIENTO EN LA RELACIÓN AGUA-SUELO-VEGETACIÓN PARA EL DEPARTAMENTO DE ANTIOQUIA. Revista EIA [en línea], no. 1, pp. 73-79. [Consulta: 27 febrero 2019]. ISSN 1794-1237. Disponible en: http://www.scielo.org.co/scielo.php?script=sci_abstract&pid=S1794-12372004000100008&lng=en&nrm=iso&tlng=es.
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Copyright (c) 2019 Gabriela Cristina Sarti, Diana N.
Effrona