Evaluation of Soil Enzymes Activities in an Araucaria–Nothofagus Forest After a Wildfire

Martínez et al. / Agro Sur 46(3):17-26, 2018 DOI:10.4206/agrosur.2018.v46n3-03

Evaluation of soil enzymes activities in an Araucaria–Nothofagus forest after a wildfire

Evaluación de las actividades de enzimas del suelo en un bosque de Araucaria–Nothofagus después de un incendio forestal

Martínez, O.a, Cabeza, R.b, Paulino, L.c, Godoy, R.d, Valenzuela, E.a

a Instituto de Bioquímica y Microbiología, Facultad de Ciencias, Universidad Austral de Chile, Campus Isla Teja, Valdivia, Chile. b Departamento Producción Agrícola, Facultad de Agronomía, Universidad de Talca, Talca, Chile. c Departamento de Suelos y Recursos Naturales, Facultad de Agronomía, Universidad de Concepción, Campus Chillán, Chillán, Chile. d Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Campus Isla Teja, Valdivia, Chile.

A R T I C L E I N F O A B S T R A C T

Keywords: enzyme activity biogeochemical processes. Soil enzymes are critical to soil nutrient cycling function and their potentialCatastrophic activities events can in be temperate sensitive bioindicators forest ecosystems, of the temperate such as wildfires,forest ecosystems alter the resilience dynamics after of Araucaria–Nothofagus forest Chilewildfire the soil enzymes activities and their relationships with soil chemical parameters in Araucaria– Nothofaguswildfire events. In this context, this is a preliminary study, which has as main objective to evaluate Original Research Article, Soil Science forest after three years of the wildfire. Soil samples were collected from 0-20 and 20- *Corresponding author: 40 cm depths, from two burnt plots (P1 and P2) and one non-burnt control plot (PC), three years Óscar Martínez after wildfire. We analyzed a composite soil sample from each plots (PC, P1 and P2) and each depth. E-mail address: andThe soilpH wasenzyme measured. activities A measuredmultiple linear were catalaseregression (CA), analysis cellulase was (CE) carried and ureaseout in (UR).order Moreover, to relate [email protected] thetotal soil nitrogen, enzymes total activities carbon, and Olsen soil phosphorous, chemical properties. total phosphorous, The results sum showed of exchangeable that the enzymes bases activities did not show any evident seasonality. On the other hand, the multiple lineal regression analysis demonstrated a weak association between the soil chemical parameters and the CA activity

preliminary conclusion, soil UR activity could be a potential bioindicator of the alterations provoked (R² = 0.47) andAraucaria–Nothofagus CE activity (R² = 0.20), and a strong association with the UR activity (R² = 0.83). As a . by wildfire in forests, as three years post-wildfire there are still differences in its activity between burnt and non-burnt plots RESUMEN procesos biogeoquímicos. Las enzimas del suelo son fundamentales para el ciclaje de nutrientes y sus actividades potenciales puedenEventos ser catastróficos bioindicadores en los sensibles ecosistemas de la resiliencia de bosques de templados,los ecosistemas como de losbosques incendios templados forestales, después alteran de eventos la dinámica de incendios de los del suelo y sus relaciones con los parámetros químicos del suelo en un bosque de Araucaria–Nothofagus después de tres años forestales. En este contexto, en este estudio preliminar, que tuvo como objetivo principal evaluar las actividades de las enzimas de incendio forestal. Las muestras de suelo fueron recolectadas a una profundidad de 0-20 y 20-40 cm, desde dos parcelas quemadas (P1 y P2) y una parcela de control no quemada (PC), tres años después de un incendio forestal. Se analizaron lamuestras suma de compuestas bases intercambiables de cada parcela y el pH.(PC, Se P1 realizó y P2) y un cada análisis profundidad. de regresión Las actividades lineal múltiple enzimáticas para relacionar del suelo las medidas actividades fueron de lascatalasa enzimas (CA), del celulasa suelo y(CE) las ypropiedades ureasa (UR). químicas Además, del se midió suelo. el Los nitrógeno resultados total, mostraron el carbono que total, las el actividades fósforo Olsen, de lasel fósforo enzimas total, no mostraron ninguna estacionalidad evidente. Por otro lado, el análisis de regresión lineal múltiple demostró una asociación lasdébil alteraciones entre los parámetros provocadas químicos por los incendios del suelo forestalesy la actividad en losCA bosques(R² = 0,47) de yAraucaria la actividad–Nothofagus CE (R² = 0,20),, ya que y unatres asociación años después fuerte de con la actividad UR (R² = 0,83). Como conclusión preliminar, la actividad UR del suelo podría ser un bioindicador. potencial de

Palabraslos incendios clave forestales: actividad existían enzimática; diferencias incendios en suforestales; actividad Araucaria entre parcelas–Nothofagus quemadas, Chile y .no quemadas

SOIL SCIENCE 17 Martínez et al. / Agro Sur 46(3):17-26, 2018

INTRODUCTION In Chile these biological processes of the soil, as po tential indicators of alteration, still have not been duly Temperate forest ecosystems normally have a li - mited access to macronutrients, as is the case for the humid forests in central and southern Chile, which to a- sioninvestigated. was an Inimportant 2002 a great area extension of Araucaria–Nothofagus of natural forest high degree depend upon internal biological processes was severely affected by burnings. Part of this exten- et al. et fragile ecosystems and the dependence upon internal al., processesforest (CONAF, in the 2002). nutrient Given cycle, the knowledgevulnerability about of these the suchin their as thenutrient Araucaria–Nothofagus cycle (Vitousek forests,, 1998; are Pérezadapted soil enzymes activities is a potential tool for monito 1998). Moreover, these mountain chain ecosystems, ring the capacity of these forests to recover and adapt nism and storms, which contribute to a regular dyna to catastrophic events of great magnitude. The aim of- to exogenous catastrophic events, such aset fires, al., volca- the present study is to preliminary evaluation the soil Despite these adaptations, the responses of the biolo- gicalmic of processes these forest to catastrophic communities events (Veblen like this are 1995). still not known. These reactions could serve as indicators- enzymes activities of catalase (CA), cellulase (CE) and of the ecosystem’s resilience against alterations. The nutritionalurease (UR) status as potential in Araucaria–Nothofagus bioindicators of ecosystems forests Araucaria–Nothofagus forest is affected by natural alte resilience after wildfire, and their relation to the soil’s rations, burning being a very important adjustment in et al., 1995; Gon- MATERIALSaffected by highly AND severeMETHODS wildfire. zález et al., biogeochemicalthe dynamics of theseprocesses forests through (Veblen the loss of organic- Study site description 2005). The forest wildfires alter the soil’s et al The study area is located in the Tolhuaca Natio cessesmatter and thethe oxidationenzyme activityand volatilisation of the soil of are nutrients highly (Caon ., 2014). For this reason, the microbial pro- - et al., nal Park (38° 10’ to 38° 15’ and 71° 40’ to 71° 50’) in sensitiveThe soil the enzymes event of activities a wildfire are due an to integrating loss of organic indi the Andes mountain chain of central-southern Chile, catormatter of (Jimenez the biological activity 2002). and the physical and che inwhich Araucaria–Nothofagus was affected by a forest wildfire in February, one mical conditions, which permits the evaluation of the- 2002 (CONAF, 2002). Three plots of land were defined2 microbial capacity in the catalytic processes, as well- stands, each of 1000 m as the availability of nutrients by means of enzymatic control plot (PC) not affected by fire, located at 1440 m et al et al level.a.s.l., andThe twosoil ofplots the affected area is an by Andisol, fire: P1, derived located from at 1160 as importance of certain soil enzymes has been described, hes,m above scoria sea and level lava y from P2, locatedthe Tolhuaca at 1240 and m Lonquimay above sea suchprocesses as catalase, (Reyes cellulase., 2011; and Cardoso urease, serving., 2013). as indi The - cators of the biological activity of the soil in the event of et- volcanoes (Pollmann, 2001). The climate is cold tempe- al., et al., et al., rate. The mean annual temperature is 8.6 °C, the maxi- Ureasealterations comes (García mainly and from Hernández, plants 1997;and microbes, Smethurst and mum and minimum mean of the coldest month is 6.7 plays1998; an indispensable Saviozzi role 2001; in theLevi-Minzi soil nitrogen cycling2002). and -2.6 °C, respectively (Pollmann, 2002). The sum- et al mer period (January) is dry, with a mean temperature of 15.1 °C. The annual precipitations are in the range process (Lillo ., 2011). The cellulase activity is re- Soilof 2500-3500 sampling mm, procedure concentrated to the winter months. lated to the carbon cycling of the soil, specifically in the foundplant residuesin all aerobic incorporation bacteria and into most the facultative soil (Deng anae and A seasonal soil sampling was performed during robes,Tabatabai, but absent 1995). in Catalase obligate is anaerobes, an intracellular and has enzyme been et al. - to carry out a chemical characterization and mea surement2004 (summer, of the autumn,enzyme winteractivity andof the spring) soil. For in ordereach cantlyused as higher an indicator in the soil of soil of tropical fertility forests(Zhang as compared, 2005). - The level of activity of these enzymes was signifi- et al., respectively.experimental Theplot (PC,samples P1 and were P2), transported two composite in soilpo forests,with deforested a decrease areas in the and urease crop farmsactivity in in Asia the (Dineshsoil has samples were taken at 0-20 cm and 20-40 cm depth, 2004a). In European Mediterraneanet coniferous al., - lyethylene bags in insulating boxes. The collected soil been verified after natural fire (Hernández 1997). was passed through a 2-mm sieve, homogenized and downIn oak-hickory process in forests the soil, the underwent activity of a reduction β-glucosidase, after a stored at 4 °C. The soil enzymes analyses were perfor- cellulase acting in the final stage of the cellulose break- chemicalmed during analysis. the first week following the sampling. One part of the sieved soil was air-dried for its subsequent prescribed fire (Boerner and Brinkman, 2003). SOIL SCIENCE

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Analytical determinations of the chemical 4 g h -1 -1 properties of the soil 4 per gram of dry soil after 1 hour of incubation. TheEach UR activity one of the(mg enzymes N-NH was) determinedis expressed indepen in mg of The chemical properties of soil samples, such as, to dentlyN-NH and by triplicate. - - Statistical analysis tal nitrogen (total N), total carbon (total C), Olsen phos- analyzedphorus (Olsen-P), using the totalmethods phosphorus described (total by Sadzawka P), sum ofet The values of the soil enzymes activities were analy alexchangeable bases (SB) and pH (1:2.5) in water, were zed using an ANOVA test and the differences between the means were analyzed by the Tukey test. Moreover, rela- Soil. (2006) enzymes and officiallyassay activities recommended for Chilean soils. tionships between soil enzymes activities and soil chemi - gression analysis. The analyses were carried out using the- mined by the manometric technique, in accordance cal properties were explored using a multiple linearp re- withThe the catalase method (CA;described EC 1.11.1.6) by Steubing activity et wasal. deter- mL g min RESULTSStatistica program AND DISCUSSION v.6.0. All analyses consider a ≤ 0.05. mL of liberated O per gram-1 of -1dry soil per minute. (2002). The The CA activity (O2 ) was expressed by the 2 Chemical characterization of the soil accordance with the method described by von Mersi cellulase (CE; EC 3.2.1.4) activity was determined in values of the chemical variables measured during the hand Schinner (1993), utilizing carboxymethyl cellulose-1 studyTable period 1 presents for the thetwo maximum, depths and minimum the different and plots:mean (Merck)-1 as a substrate. The CE activity (mg GLC g 24 ) is expressed in µg of glucose equivalents per gram geable bases. The values of the measured chemical pa methodof dry soil described in 24 hours by Steubingof incubation. et al The urease (UR; EC rameterspH, total C,correspond total N, Olsen-P, to values total observedP and sum in of previous exchan- the3.5.1.5) quantity activity of ammonium was determined formed in accordanceafter the addition with the of - . (2002), measuring et al et al studies of Chilean volcanic ash-derived soil (Pollmann, urea (Merck) as a substrate, incubating for 2 h at 37 °C. 2001; Valenzuela ., 2002; Alvear ., 2007).

Table 1. Araucaria–Nothofagus forest soils from Tolhuaca National Park. Soil chemical properties measured at 0-20 and 20-40 cm depths from control plot (PC) and two burning (P1 and P2) Cuadro 1. Araucaria–Nothofagus en el Parque Nacional Tolhuaca. Propiedades químicas del suelo medidas a profundidades de 0-20 y 20-40 cm desde la parcela de control (PC) y dos parcelas suelos afectadas por el fuego (P1 y P2) en suelosPC de bosque de P1 P2 0-20 cm depth max Min mean max min mean max min mean 5.47 5.47

Water pH (1:2.5) 5.60 5.30 5.70 5.20 5.70 5.30 5.50 Total carbon (%) 14.70 13.60 14.23 14.30 12.90 13.37 11.40 10.40 10.87 Total nitrogen (%) 0.44 0.15 0.28 0.45 0.23 0.31 0.39 0.17 0.31 -1 Olsen phosphorous (mg kg ) 3.30 2.90 3.03 5.50 3.30 4.20 2.00 2.00 2.00 -1 kg 1.9 Total phosphorous (mg kg ) + 1466 1396 1440 1576 1064 1357 1845 1279 1485 -1 Sum20-40 exchageable cm depth of bases (cmol ) 1.3 0.8 1.0 0.9 1.3 0.9 0.7 0.8

Water pH (1:2.5) 5.70 5.50 5.60 6.00 5.60 5.87 6.00 5.80 5.90 Total carbon (%) 11.50 9.00 10.03 10.20 5.50 7.93 10.20 6.70 8.20 Total nitrogen (%) 0.40 0.19 0.32 0.42 0.20 0.27 0.37 0.27 0.30 -1 Olsen phosphorous (mg kg ) 2.00 2.00 2.00 2.00 2.00 2.00 2.10 2.00 2.03 -1 kg Total phosphorous (mg kg ) + 1530 1193 1329 1824 1352 1643 1377 1247 1313 -1 Sum exchageable of bases (cmol ) 0.7 0.4 0.5 1.3 0.9 1.0 0.8 0.5 0.7 SOIL SCIENCE 19 Martínez et al. / Agro Sur 46(3):17-26, 2018

Soil enzymes activities increase in CA activity in the burnt plots is probably related to a stabilization of the soil’s aerobic microbio mL et al g min - 2 -1 The -1CA activity variedp between 0.50 and 0.99 O GLClogical g population post-fire (Vázquez ., 1993). in the superficial 20 cm (Figure 1). In gene- withThe increasing-1 CE activity-1 depth, varied CE between activity diminished 101.2 and 788.9 to a ran mg ticallyral, significantly during the higher sampling ( ≤ 0.05)period. values Nevertheless, were obtained with 24 h at 0-20 cm depth (Figure, probably 2). due However, to the increasingfor the CP andsampling P1 0-20 depth, cm, thewhich CA doactivity not differ diminished statis- lower SOM content, as discussed-1 -1 for CA activity. These- mL g min , which has been results,ge of 62.7-537.6 coincide mgwith GLC reports g 24 hby other authors, who related to a decrease in the the -1soil’s -1content of organic to values of 0.32-0.79 O2 son of the year had no obvious observable effect on the indicate that a minor cellulose content, a low oxygen CAmatter activity, (SOM) though (Johnson showing and a Temple, weak tendency 1964). Thetowards sea- diffusion and low availability of nitrogen, influence CE a minor activity in autumn and winter. There was no activity (Wagner and Wolf, 1998). In summer, the highest CE activity was reported in PC at 0-20 cm, and the plots and the control plot, indicating that the effect of lowest was reported in spring. P1 0-20 cm presented significant difference in CA activity between the burnt presentthe highest differences activity inbetween autumn, the while different the P2 seasons 0-20 cm, of The restoration of the CA activity from the effects of the PC 20-40 cm, P1 20-40 cm and P2 20-40 cm did not the fire would not have any influence after two years. no effect of the climatic season on the CE activity was et al. observed.the year (Figure Nevertheless, 2). In accordance Fioretto et al.with these results, infire Picea under balfouriana the study conditions, contradicts the reports seasonal variations of the CE activity in Mediterranean by Zhang (2005), who found that the CA activity soils with predominating Cistus incanus (2005), L. vegetation, reported forests eight years post-fire is still sensitive to the alterations provoked by the fire. The

Summer Autumn 1.2 1.2 ) 1 - 1.0 1.0 min 1 -

g 0.8 0.8 mL

2 0.6 0.6 (O 0.4 0.4

0.2 0.2 Depth Catalase 0.0 0.0 0 - 20 cm 20 - 40 cm Winter Spring 1.2 1.2 ) 1 - 1.0 1.0 min 1 -

g 0.8 0.8 mL

2 0.6 0.6 (O 0.4 0.4

0.2 0.2 Catalase 0.0 0.0 PC P1 P2 PC P1 P2

Figure 1. Araucaria–Nothofagus

Catalase (CA) activity in different seasons of forest at 0-20 and 20-40 cm soil layers. Enzyme Figura 1. Araucaria–Nothofagus en profundidades de suelo activity values are expressed as mean ± SD. (PC, control plot; P1 and P2, burnt plots). (n = 72). Actividad de la catalasa (CA) en diferentes estaciones del bosque de 0-20 y 20-40 cm. Los valores de la actividad enzimática se expresan como media ± DS. (PC, parcela control; P1 y P2, parcelas quemadas). (n = 72). SOIL SCIENCE

20 ..... the highest values being observed in autumn and sults showed a slight seasonal tendency, where for all the plots a major activity was registered in summer intensity. Moreover, Palese et al and a minor activity in spring, a period when snow inspring soils and with the typical lowest Mediterranean in summer, independently vegetation the of sea fire accumulated in the study zone. The UR activity in the . (2004), reported that p minish in autumn and increase in spring, can be modi- in the PC plot, as compared with the burnt plots P1 and sonal variation in β-glucosidase activity, tending to di- superficial 0-20 cm, was significantly higher ( ≤ 0.05) - of the UR activity to diminish in zones affected by bur fied by the effect of the temperature in the soil reached P2 (Figure 3). Previous studies confirm the tendency during the fire. No statistical differences of CE activity et al - thewere recolonization observed between of the thesoil control of the burntplot (PC) plot andby fun the otherning, becausehand, Lillo as eta consequenceal of the fire, the organic giburnt populations, plots (P1 and/orbeing the P2). main This producers could be attributed of cellulase to ureaseforms ofactivity N oxidize showed (Hernández a similarity in .,the 1997). middle On zone the et al - of the altitudinal transect,. (2011) Conguillío reported National that the Park,levels fa of vored by the accumulation of organic matter. (Martínez ., 2006). - 4 g h were registered in the samples from the Regarding-1 -1 the UR activity, values of 58.5-277.7 mg Relationships between soil enzymes activities and N-NH 4 g soil chemical parameters h0-20. The cm observeddepth (Figure decrease 3). This of URactivity activity diminished with increa with-1 singdepth-1 soil (20-40 depth cm) may to be values related of 86.3-198.1 to a minor mgtemperature N-NH The results of the multiple linear regression analy et al - sis show that the CA activity presents a low correlation cm depth, were higher during the whole sampling pe - (Reyes ., 2011). The UR activity values for PC 0-20 - coefficient with regard to the chemical properties of riod, as compared with P1 and P2 (Figure 3). The re- the soil considered in this study (Table 2). The multiple

Summer Autumn 1000 1000 ) 1 -

24 h 800 800 1 -

600 600 GLC g g µ

( 400 400

200 200 Depth Cellulase 0 0 0 - 20 cm 20 - 40 cm Winter Spring 1000

) 1000 1 -

24 h 800 800 1 -

600 600 GLC g g µ

( 400 400

200 200 Cellulase 0 0 PC P1 P2 PC P1 P2

Figure 2. Araucaria–Nothofagus

Cellulase (CE) activity in different seasons of forest at 0-20 and 20-40 cm soil layers. Enzyme Figura 2. Araucaria–Nothofagus en profundidades de suelo de activity values are expressed as mean ± SD. (PC, control plot; P1 and P2, burnt plots). (n = 68). Actividad de celulasa (CE) en diferentes estaciones del bosque 0-20 y 20-40 cm. Los valores de la actividad enzimática se expresan como media ± DS. (PC, parcela control; P1 y P2, parcelas quemadas). (n = 68). SOIL SCIENCE

21 Martínez et al. / Agro Sur 46(3):17-26, 2018

Summer Autumn 300 300 ) 1 -

h 250 250 1 - g

4 200 200 NH -

N 150 150 g µ ( 100 100

50 50 Depth Urease 0 0 0 - 20 cm

20 - 40 cm Winter Spring 300 300 ) 1 -

h 250 250 1 - g

4 200 200 NH -

N 150 150 g µ ( 100 100

50 50 Urease

0 0 PC P1 P2 PC P1 P2

Figure 3. Araucaria–Nothofagus

Urease (UR) activity in different seasons of forest at 0-20 and 20-40 cm soil layers. Enzyme Figura 3. Araucaria–Nothofagus en profundidades de suelo de activity values are expressed as mean ± SD. (PC, control plot; P1 and P2, burnt plots). (n = 72) Actividad de ureasa (UR) en diferentes estaciones del bosque 0-20 y 20-40 cm. Los valores de la actividad enzimática se expresan como media ± DS. (PC, parcela control; P1 y P2, parcelas quemadas). (n = 72).

Table 2. between the soil enzymes activities and chemical properties. C, total N, P and K in mangrove forests. On the other Correlation coefficient for the models adjusted Cuadro 2. found a significant correlation between CA and organic ajustados entre las actividades de las enzimas del suelo y las propiedades Coeficiente químicas. de correlación para los modelos hand, Frankenberger and Dick (1983), did not find any significant correlations between CA and a number of Adjusted R2 chemical soil parameters (pH, organic C, total N and *** capacity of cationic exchange) analyzing ten series of Catalase Level of significance fense mechanism of the aerobic microorganisms facing non-cultivated soil in California. The CA activity is a de- Cellulase * 0.47 0.000 content of the soil. However, literature is scarce with *** Urease 0.20 0.018 regardoxidative to thisstress, point. probably independent of the C and P * ** *** , , 0.83 0.000 spectively. multiple regression analysis it was necessary to trans significant at the 0.05, 0.01 and <0.01 level of probability, re- In order to fulfill the assumption of normality for the between CE activity and the chemical properties of the- form the CE activity data (Log10 data). The correlation

soil is very low (Table et2), al. the pH, Olsen-P and SB, being linear regression coefficients (Table 3), showed that the coefficients of importance in the regression model ofthe bases CA activity and total model N. is explained mainly by the regres- Cepeda(Table 3). et Anderssonal. (2004), found a significant sionLeirós coefficient et al corresponding to Quercusthe parameters forests locasum betweenrelation between CE and total CE and C and the N.C:N On relation, the other while hand, Trasar- Gar (1998), obtained significant correlations . (2000), studying - - availableted in Galicia, Ca and found K+ significant correlationset al. between cía and Hernández (1997), obtained a significant correet al.- CA activity and2+ total N and C content, C/N relation and lation between the β-glucosidase activity (a cellulase) . Whereas Dinesh (2004b) and the organic matter of the soil, as did Jimenez SOIL SCIENCE

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Table 3. et al et al zymes activities and soil chemical parameters. demonstrated the correlation between the UR acti Multiple regression coefficients between soil en- Cuadro 3. Jimenez . (2002) and Baligar . (2005), et have al. dades de las enzimas del suelo y los parámetros químicos del - suelo. Coeficientes de regresión múltiple entre las activi- vity and the total N and C content, while Zantua nic(1977), C. The and strong Frankenberger correlation andbetween Dick the(1983) chemical have pare- Catalase Cellulase Urease rametersported significant and the UR correlations activity is betweencoherent URwith and the orga sen- Intercept NS NS ** - - pH w NS * ** -0.689 -2.463 -690.798 sitivity of this enzymeAraucaria–Nothofagus activity to the effect ecosystemof the fire * NS *** Total N 0.164 0.799 115.210 in the 0-20 cm depth, being greatest in the unaltered NS NS *** ecosystem (PC). The Total C 0.561 -0.620 -290.597 has a limited access to N (Lusk, 2001), the UR activi- NS ** 5.174 NS resulting from animal metabolism, and urea analogous 0.007 0.067 23.933 ty being involved in the use of organic nitrogen (urea NS NS NS Olsen-PTotal P 0.055 -0.191 correlation between UR activity and total N and C con compounds). This is probably the reason for the strong -0.000 *** -0.000 ** -0.013 * et al bases In the case of CA and CE there is a weak correlation- Sum of exchangeable *, **, *** 0.301 0.441 37.950 betweentent (Trasar-Cepeda the estimated and., 1998). the observed activity of the

significant at the 0.05, 0.01 and <0.001 level of probability, re- would be necessary to study the relation between the spectively. NS, not significant. fractionsenzymes ofCA, the CE measured and UR (Figurechemical 4). parameters, For CA and such CE asit soluble C, soluble P and mineralizable N. Though, there is a better adjustment of the UR activity behaviour mo del. Here it is possible to observe differences between less,(2002), Lillo who et reportedal a significant correlation between the plots; the data is arranged according to the magni- rrelationβ-glucosidase between and CEtotal and N, the pH contentand organic of organic C. Neverthe matter- tude of the chemical soil parameters considered in the of the soil, neither. (2011) with did the not pH. find The any weak significant association co- study. - between the CE activity and the chemical parameters of the soil measured in this study, are in agreement pose of evaluating the association of the enzyme activi with similar results obtained by Balota et al. This is a first exploratory study, which has the pur- - CE and a number of chemical parameters in agricultu (2004), ty of the soil post-wildfire,Araucaria–Nothofagus with a few chemical soilforests va- who did not find any significant correlation between inriables the Andes (total mountain.N, total C, Thetotal objective P, Olsen-P, of sum correlating of exchan va- It seems that the low correlation between the chemi- riablesgeable basesdoes not and have pH) a in predictive purpose. Its only pur calral parameterssoils (pH, P, ofCa, the Mg, soil CEC and and the saturationCE activity ofwould bases). be pose is to observe the relation between the parameters- related to the type of temperate forest vegetation, and- that could affect the enzyme activity. Finally, the purpo- et al., se of this investigation has been to report the events in the Araucaria–Nothofagus - dependenttherefore with on the the synergism type of organic occurring matter between (Lillo the di claim to predict the behaviour of the enzymes facing 2011). Moreover, the degradation of cellulose is highly changes in the levels of chemical forest post-firesubstances and in does the soil. not - fferent enzymes of the cellulolytic complex (Bhat and CONCLUSIONS teBhat, forests 1997). is the On presence the other of hand, trace aelements, factor that such could as e.g. be influencing the CE activity in the soils of these tempera- The main preliminary conclusions of this study

Al (III) and Fe (II), probably forming complexes with SOM,In inrelation this way to the inhibiting UR activity, the enzymethis has aactivity high and (Deng sig were: (i) no seasonality could be determined regarding and Tabatabai, 1995). theresoil enzymes were no activities; differences (ii) thebetween soil enzymes the control activities plot p - of CA, CE and UR decreased with increasing depth; (iii) nificant association with the chemical parameters of the soil ( ≤ 0.05). This model explains 83% of the UR detection(PC) and theof changesburnt plots in the (P1 activity and/or ofP2) these regarding enzymes CA activity (Table 2). In this adjusted model, the significant and CE activities, therefore, three years post-fire the multiple regression coefficients correspondet al to total N, rameters measured in this study are not associated in studiedtotal C, SB the and UR pH, activity whereas in response total P and to Olsen-Pthe application are not thedoes same not possessway with sensibility; the enzyme (iv) activity the soil of chemical CA, CE andpa- significant. With regard to this, Baligar . (2005), et al of P, their results showed a non-significant correlation UR respectively; (v) the UR activity is regulated by the coefficient. The studies of Trasar-Cepeda . (1998), chemical parameters of the soil; (vi) UR activity could SOIL SCIENCE

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Predicted v/s Observed a Predicted v/s Residuals b 1.2 0.4 )

-1 1.0 0.2 min -1 0.8 PC 0-20 PC 20-40 mL g

2 P1 0-20 0.6 PC 0 - 20 0.0 P1 20-40 PC 20-40 Residuals P2 0-20 0.4 P1 0-20 P2 20-40 P1 20-40 -0.2 0.2 Observed (O P2 0-20 P2 20-40 0.0 -0.4 0.0 0.2 0.4 0.6 0.8 1.0 1.2 0.0 0.2 0.4 0.6 0.8 1.0 1.2

-1 -1 -1 -1 Predicted (O2 mL g min ) Predicted (O2 mL g min )

Predicted v/s Observed a Predicted v/s Residuals b 3.0 1.0 )

-1 0.8 h 0.5

24 2.5

-1 PC 0-20 0.3 PC 20-40 P1 0-20 2.0 PC 0 - 20 0.0 P1 20-40

PC 20-40 Residuals -0.3 P2 0-20 P1 0-20 P2 20-40 1.5 P1 20-40 -0.5 P2 0-20

Observed (µg GLC g GLC (µg Observed -0.8 P2 20-40 1.0 -1.0 1.0 1.5 2.0 2.5 3.0 1.0 1.5 2.0 2.5 3.0 Predicted (µg GLC g-1 24 h-1) Predicted (µg GLC g-1 24h-1)

Predicted v/s Observed a Predicted v/s Residuals b 300 80 ) -1 250 60 h -1

g 40

4 PC 0-20 200 20 PC 20-40 P1 0-20 150 PC 0 - 20 0 P1 20-40 PC 20-40 Residuals -20 P2 0-20 100 P1 0-20 P2 20-40 P1 20-40 -40 50 P2 0-20 Observed (µg NH-NH -60 P2 20-40 0 -80 0 50 100 150 200 250 300 0 50 100 150 200 250 300

-1 -1 -1 -1 Predicted (µg NH-NH4 g h ) Predicted (µg NH-NH4 g h )

FigureF i4.gure 4. Relationship between A) catalase (n = 54), B) cellulose (n = 54) and C) urease (n = 54) with chemical parameters of Figura 4 the soil; model adjusted for observed versus predicted data (a); model adjusted for residuals versus predicted data (b). . Relación entre A) catalasa (n = 54), B) celulosa (n = 54) y C) ureasa (n = 54) con parámetros químicos del suelo; modelo ajustado para los datos observados frente a los previstos (a); Modelo ajustado por residuos frente a datos previstos (b). 24

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24 ..... be a potential indicator of the alterations provoked by bed and disturbed mangrove forest of South Andaman Araucaria–Nothofagus forests, as three fire in soils of (India). Wetlands Ecology and Management 12, 309- years post-fire there are still differences in its activity enzyme320. activities and microbial growth and activity in Frankenberger, W.T., Dick, W.A., 1983. Relationships between between burnt and non-burnt plots. Acknowledgements: - dices in soil. Soil Science Society American Journal 47, We thank the Corporación Na- thank Äsa Kjellgren for English translation this manus respiration,945-951. ATP content and enzyme activities in Medi cript.cional Forestal (CONAF) of the Araucania Region. We Fioretto, A., Papa, S., Pellegrino, A., 2005. Effects of fire on soil - García, C., Hernández, T., 1997. Biological and biochemical in- REFERENCES dicatorsterranean in maquis. derelict Applied soils subject Vegetation to erosion. Science Soil 8, Biology 13-20. - Arau- Actividades biológicas y estabilidad de agregados en un caria–Nothofagusand Biochemistry 29,forests 171-177. in Villarrica National Park, Alvear,suelo M., Urra,del bosque C., Huaiquilao, templado R., chileno Astorga, bajo M., Reyes,dos etapas F., 2007. su González, M., Veblen, T., Sibold, J., 2005. Fire history of cesionales y cambios estacionales. Revista de la Ciencia - Chile. Journal of Biogeography 32, 1187-1202. Hernández,gical properties T., García, ofC., MediterraneanReinhardt, I., 1997. pine Short-term forest soils. effect Bio medel Sueloactivities y Nutrición in leaf litter, Vegetal humus 7(3), and 38-50. mineral soil layers of wildfire on the chemical, biochemical and microbiolo- Andersson, M., Kjøller, A., Astruwe, S., 2004. Microbial enzy- - logy and Fertility of Soils 25, 109-116. of European forests. Soil Biology and Biochemistry 36, Jimenez,biochemical M., de la parameters.Horra, A.M., Pruzzo,Biology L.,and Palma, Fertility R.M., of 2002. Soils 1527-1537. Soil quality: a new index based on microbiological and Baligar,rus. V.C., Communications Wright, R.J., Hern, in Soil J.L., Science2005. Enzyme and Plant activities Analysis in soil influenced by levels of applied Sulfur and Phospho- measurement35, 302-306. of “catalase activity” in soil. Soil Science Balota, E.L., Kanashiro, M., Colozzi Filho, A., Andrade, D.S., Johnson, J.L., Temple, D.L., 1964. Some variables affecting the 36, 1727-1735. Society American Proceeding 28, 209-213. Dick, R.P., 2004. Soil enzyme activities under long-term Leirós, M., Trasar-Cepeda, C., Seoane, S., Gil-Sotresa, F., 2000. tillage and crop rotation systems in subtropical agro- Biochemical properties of acid soils under climax vege- Bhat,ecosystems. M.K., Bhat, S.,Brazilian 1997. Cellulose Journal of degrading Microbiology enzymes 35, 300- and tation (Atlantic oakwood) in an area of the European their306. potential industrial applications. Biotechnology temperate±humid zone (Galicia, NW Spain): general parameters. Soil Biology and Biochemistry 32, 733-745. Levi-Minzi,characteristics R., Saviozzi, in a A., mediterrean Cardelli, R., agricultural Riffaldi, R., area.2002. Archi Rela- enzymeAdvances activity 15, 583-620. in southern Ohio oak–hickory forests. tionships between biological and physico-chemical soil Boerner, R.E.J., Brinkman, J.A., 2003. Fire frequency and soil - tividadves of Agronomy biológica anddel Soilsuelo Science de bosque 48, 279-288. templado en un Applied Soil Ecology 23, 137-146. Lillo, A., Ramírez, H., Reyes, F., Ojeda, N., Alvear, M., 2011. Ac- Caon, L., Vallejo, V.R., Ritsema, C.J., Geissen, V., 2014. Effects of wildfire on soil nutrients in Mediterranean ecosystems. transecto altitudinal, Parque Nacional Conguillío (38º M.Y.H.,Earth-Science Santos, Reviews C.A., Alves, 139, P.R.L., 47-58. de Paula, A.M., Naka forestS), Chile. of SouthBosque America. (Valdivia), Revista 32(1), Chilena 46-56. de Historia Na Cardoso, E.J.B.N., Vasconcellos, R.L.F., Bini, D., Miyauchi, Lusk, C., 2001. Leaf life spans some conifers of the temperate - - redtani, to A.S., assess Pereira, the effects J., Nogueira, of use and M.A., management 2013. Soil health:on soil blestural y 74, grupos 711-718. funcionales de hongos presentes en suelos looking for suitable indicators. What should be conside- Martínez,de bosque O., Valenzuela, de Araucaria–Nothofagus E., Godoy, R., 2006. Poblaciones via-

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