R.C. Suelo Nutr. Veg. 10(2): 126 - 138 (2010)

BIOCHEMICAL PROPERTIES IN VASCULAR EPIPHYTES SUBSTRATE FROM A TEMPERATE OF CHILE

Francisco Reyes1,2, Silvana Zanetti3, Alejandro Espinosa4 and Marysol Alvear1,2*

1Departamento de Ciencias Químicas; Facultad de Ingeniería, Ciencias y Administración and 2Scientifical and Technological Bioresource Nucleus (BIOREN); Universidad de La Frontera, Avenida Francisco Salazar 01145, Casilla 54-D, Temuco, Chile; 3Università degli studi di Firenze, Firenze, Italia. 4Departamento de Ciencias Forestales, Facultad de Ciencias Agropecuarias y Forestales, Universidad de La Frontera. *Corresponding author: [email protected]

ABSTRACT

The temperate of south-central Chile belong to the association Lapageria aextoxiconetum Oberdorfer vegetation, dominated by Aextoxicon punctatum R. et P., elderly and multi-layered, where the strata are emergent, dominant and co-dominant, shrub and herbaceous epiphytes. This work is the first report of measurements of some biochemical properties in samples from vascular epiphytes substrate in temperate forests. We evaluated the most frequent ecological situations: bifurcated (BT), dead standing trees (SDT) and medium gap border trees (MGBT), ES were compared with the surrounding soil forest land (SS) as control. The microbial biomass and enzyme activities of substrate were higher in ES of BT, situation probably due to optimal micro-environmental conditions (moisture and humidity, temperature, organic matter (OM) content and nutrient availability); similarly, lower levels of activity were found in ES in MGBT situation. We found a statistically significant correlation (p ≤ 0.05) between evaluated microbial biomass and enzymatic activities. Furthermore, the biochemical properties were influenced by factors such as moisture, temperature, pH and OM content and all of these factors correlated significantly (P≤0.01) among them. These results demonstrate a difference between ES and SS in BT that should be explored to gain insights in understanding the processes of decomposition using the natural microcosms that ES provides.

Keywords: vascular epiphytes substrate, enzymatic activities, temperate forest.

INTRODUCTION

Temperate rainforests of southern Chile 2001). According to Arroyo et al. (1996), have a global importance based on 2 the in southern Chile outstanding aspects: the existence of is composed of 443 species of vascular continuous undisturbed forests which in with 160 woody species (44 other temperate regions of the world have species of trees corresponding to 32 practically disappeared and the genera and 20 families) and 283 extraordinary biodiversity of the region herbaceous species. More than 70% of (Armesto et al., 1998, Olson et al., forest species in southern Chile are

126 Biochemical properties in vascular epiphytes, Reyes et al. concentrated between 36° and 40º S and have no direct relationship with the soil correspond to the area of our country and that develop on stems, branches and with greater biodiversity. even leaves, as epiphytes, but they can The precipitation chemistry in Chile also be developed on rocks hence, not still reflects a close approximation of pre- directly soil to supply nutrients and industrial conditions (Godoy et al., water. On the other hand, Hernández- 2001). In this way, the productivity of the Rosas (2001) indicates that presence of ecosystem depends on the internal epiphytes is influenced by climatic and cycling of soil organic matter (SOM) biotic factors that are related to the (Vann et al., 2002, Perez et al., 2005). substrate. In the temperate forests of Chile, Epiphytes contribute to enhance the mainly located in soils with restrictive forest biodiversity (Antibus and Lesica, characteristics of nitrogen and 1990; Hernández-Rosas, 2001). phosphorus, it is absolutely necessary to Moreover, Cardelús et al. (2006) showed preserve the available nutrients and that some species of epiphytes are useful minimize the losses through gases or as change indicators in several leaching (Huygens et al., 2008 ), in those ecosystems, as well as providing , areas with high rainfall, where the nectar, water and other compounds into atmospheric N inputs are minimum. The other organisms. Therefore, they are main way to save nutrients in forests considered as an important component ecosystems in the southern hemisphere is within the structure and dynamics of the through the presence and decay of organic forest, because they have ability to matter deposited in the soil (Pérez et al., intercept nutrients within ecosystems. 2005, Schlegel and Donoso, 2008). Epiphytes have been studied in tropical Moreover, the OM improves the structure forests (Vance and Nadkarni, 1990, of the soil and its ability to retain Nadkarni et al., 2004; Higuera and humidity, which becomes a basic Martínez, 2006). Colonization of vascular condition to the productive potential of epiphytes on trees depends on the the forest (Schllegel and Donoso, 2008). characteristics of the substrate, the In these forests, there are exudation of compounds from the bark interrelationships among trees and other and/or deposit material from the organisms, as well as between certain decomposition of non-vascular epiphytes, species of grass, shrubs and animals including mosses and liverworts associated strata forming communities or (Hernández-Rosas, 2001). This interaction “subcommunities”, each of them with would be capable of further proliferation, different demands on the physical and diversity and activity of microorganisms chemical environment, to which plants together with secretion of enzymes, due to respond with adaptations as growth a rich labile carbon and nitrogen characteristics (Steubing et al., 2002), compound, supply mainly used as energy giving a structure and species sources. composition in themselves (Kimmins, Recently, Rousk and Nadskarni 1996). The epiphytism is an interspecific (2009) help understanding processes of relationship that is part of commensalism decomposition in ecosystem forest and (Smith and Smith, 2001), where one have investigated the relative importance species benefits (the epiphyte is of the two major decomposer groups supported) and the other one is (fungi and bacteria) in canopy and forest unaffected (Donoso, 1992). Granados soils of a North American temperate wet and Tapia (1990), described plants that forest.

127 R.C. Suelo Nutr. Veg. 10(2): 126 - 138 (2010)

On the other hand, the organisms common ecological situations (BT, DST represented by a small fraction of soil and MGBT) compared with the OM are responsible for mineralization surrounding soil. We hypothesize that the processes (Vance et al., 1987; Vance and biochemical properties of vascular Nadkarni 1990). Microbial biomass in epiphytes substrate are affected by soil is a catabolic agent of ecological conditions of the host trees. biogeochemical processes and energy and nutrient reservoir, but very susceptible to changes in land use and MATERIALS AND METHODS physicochemical characteristics of the environment. It determines the balance of ecosystem productivity (Galantini and Site characteristics

Suñer, 2008). There are early biological The study was carried out in Rucamanque indicators such as fluorescein diacetate (38° 39'S, 72° 35'W), Araucanía Region, (FDA) hydrolysis, which quantifies Chile (Figure 1). It has an area of 435 ha, active microbial biomass (Alvear et al., an average altitude of 376 m, being 62% 2008), the C and N biomass (MBC and of its area between 201 and 400 masl. The MBN, respectively), whose climate is temperate and humid, with an determination shows the size of the average annual temperature and rainfall of microbial community present in 1,400 mm and 12ºC, respectively (Zúñiga substrates and soils (Alvear et al., 2007; et al., 2008). Alvear et al., 2008). Moreover, Zagal et The selected forest vegetation belongs al. (2002) indicate that MBC and MBN to the Lapagerio Aextoxiconetum constitute an essential measure of Oberdorfer association, dominated by ecological importance, since one part Aextoxicon punctatum R. et P., the oldest represents the level of biological activity and multi-layered, where there are involving the labile component of OM emerging strata (mainly Nothofagus and the other, integrating environmental obliqua (Mirb) Oerst.) dominant and factors and their influence on it. In codominant (consisting of tolerant species addition, hydrolytic enzymes, such as and semitolerant as Aextoxicon acid phosphatase, involved in the cycle punctatum, Persea lingue (R. et P.) Ness, of phosphorus and the urease, involved in Weinmannia trichosperma Cav. and the nitrogen cycle, play a fundamental Laureliopsis philippiana (Phil) Losser), role in the cycling of nutrients for growth shrub, and herbaceous epiphytes (San and for maintenance of vascular Martín et al., 2008). epiphytes in the forest ecosystems (Vance and Nadkarni, 1990; Hernández-Rosas, Sampling Design 2001; Nadkarni et al., 2004). Measurement of biochemical Within a 1,000 m2 plot of a addressed parameters (Alvear et al., 2007) allow to random was raised, 30 mature trees analyze the interaction between the ES, (DHB≥ 10cm) were sampled in order to in respect to the ecological function, identify the vascular epiphyte vegetation especially the relationship between on the shafts of two forest species and to nutrients and habitat conditions. characterize the forest compositional This work is the first report of a variation, considering both the temperate forest of Chile that considers phorophytes species and the most measurements of some biochemical frequent colonization situations. Three properties in ES in the three most mature trees for the more frequent

128 Biochemical properties in vascular epiphytes, Reyes et al.

Legend Stream Rucamanque Forest

Temuco

Meters 0 750 1500

Figure 1. Study site location, vegetation belonging to the association Lapagerio aextoxiconetum Oberdorfer, south-central Chile (38° 39'S).

colonization situations were selected, were moved to the laboratory in from which epiphytes substrate (ES) isothermal bags, sieved (< 2 mm) and samples and surrounding soil forest land stored at 4°C for later analyses, which (SS) were extracted. The most frequent were performed within 20 days after situations for colonization taken into sample collection. account were: a) bifurcated trees (BT), Analytical results were made in represented for A. punctatum species with triplicate and were calculated on the basis organic matter accumulation; dead of oven-dried weight at standard standing trees (DST), all of them temperature (105ºC). belonging to A. punctatum; and medium gap border trees (MGBT) (≤ 500m²) of N. Assessment of vascular epiphyte obliqua species. Three ES and SS samples vegetation representing each most frequent situation Attributes of the vascular epiphytic flora for colonization were collected during were evaluated: species present in each 2006 autumn season. The SS samples settlement on the shaft (Hernández-Rosas, were collected at 0-15 cm soil depth and 2001), coverage through the projection on ES sampling plots size were 250 cm2 and the shaft of each of the present vascular were located on the longitudinal axis of epiphyte species (Margalef, 1998; colonized shafts, with a distance between Hernández-Rosas, 2001) and sociability, plots of 75 cm. In BT ecological situation, which identifies the type of grouping that the three plots were located next to each showed the species, indicated through other along the bifurcation. The simple observation. average distance between the samples for each situation was 20 meters, except for Determination of hydrolysis of FDA, MGBT, where the average distance was 5 MBC and MBN meters. ES samples were difficult to obtain and that´s was the reason for not FDA hydrolysis was performed according take over 50 g in each sample. Samples to the method described by Alvear et al.

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(2008), expressing results as µg of demo version of SPSS 11.0 software for fluorescein g-1. Microbial biomass C Windows was used. (MBC) and N (MBN) were determined according to the fumigation-extraction method (Vance et al., 1987). Carbon RESULTS concentration of fumigated and non- fumigated samples was determined through oxidation with potassium Tree and epiphytic species dichromate and the difference was divided characterization by the recovery factor Kec=0.45 (Joergensen, 1996). Nitrogen Aextoxicon punctatum was the main concentration was calculated as the species tree inside the plot, while other difference of reactive N to ninhydrin of species, such as N. obliqua, Eucryphia fumigated and non-fumigated samples cordifolia Cav., L. philippiana and P. through the colorimetric method lingue, had a much more limited presence. (Joergensen and Brookes, 1990). Biomass Nothofagus obliqua is deciduous while A. N values were calculated by using punctatum has abundant and dense K =0.54 (Brookes et al., 1985). The foliage, which lowers the brightness en inside the forest. However, the lighting of results were expressed as μg C g-1 and μg the tree tops in most of these was full, N g-1 for the MBC and NBM, belonging to the dominant canopy layer. respectively. The rest of them corresponded to the Determination of enzyme activities emerging class these are trees that go beyond the dominant stratum and are Acid phosphatase activity (EC 3.1.6.1) noted for their height. N. obliqua, E. was determined according to the method cordifolia and some individuals of A. outlined by Alvear et al. (2008), and this punctatum and L. philipiana belong to -1 activity was expressed as μmol PNP g this class. -1 h . Urease activity (EC 3.5.1.5.) was The type of shaft was a factor that determined using to the modified method could influence the colonization of of Alvear et al. (2008) and the data were epiphytic species). The species A. -1 -1 expressed as μmoles NH3 g h . punctatum evaluated in two situations had a type called smooth bark, which has no Experimental design and statistical large cracks or fissures, while N. obliqua analyses had cracked and rough shaft. An addressed random sampling was The identified vascular epiphyte raised. Variables for biochemical species were mainly ferns. It was possible properties and physical-chemical factors to observe that Asplenium dareoides A.N. showed no normality assumption being Desv., Hymenoglossum cruentum (Cav) transformed yet by natural logarithm Presl and Hymenophyllum cuneatum function, so they were subjected to the Kunze are the only species that are not nonparametric Kruskal-Wallis test to common to the 3 assessed situations. With determine whether there were significant respect to coverage of epiphytic species, it differences, with a significance level of is important to note that Hymenophyllum 95% (P≤0.05). The level of correlation caudiculatum Mart and H. cuneatum between biological activities was made by species were recorded 75 % above cover Pearson's test with a significance level of values. Sociability was an attribute of the 99% (P≤0.01). For statistical analysis the epiphytic vegetation evaluated in field.

130 Biochemical properties in vascular epiphytes, Reyes et al.

By the way, A. dareoides was the only C (Table 1). However, when comparing species with growth evaluated in the ES in three evaluated situations no situations. Besides, the number of plants significant differences (P>0.05) were recorded for the same species was quite observed. The moisture (Table 1) showed low, since plants mainly developed at the significant differences (P≤0.05) various base of the shafts (San Martín et al., 2008; situations, obtaining higher moisture Zanetti, 2004). Unlike, H. cuneatum and levels in BT situation with an average of H. caudiculatum were the only species 63.5% and 55% in ES and SS, that were found growing in almost pure respectively. Lower moisture levels were populations. obtained in the MGBT situation, due to the presence of a gap in the forest. In Soil and epiphytes substrate relation to OM content, significant physicochemical properties differences (P≤0.05) in BT and MGBT situations were observed (Table 1). A significant (P≤0.05) average soil The P availability showed significant temperature was observed (Table 1) when differences (P≤0.05) in the various comparing SS in different situations, assayed ecological situations, having a reaching higher temperatures in the ES, greater availability in the BT and DST whose values were among 14.8 and 16.8° situations, both in ES and SS.

Table 1. Physicochemical parameters in epiphytes substrate (ES) and surrounding soil forest land (SS) for three ecological situations in a temperate forest from south-central Chile.

BT Situation DST Situation MGBT Situation ES SS ES SS ES SS LSD Olsen P (mg kg-1) 9.9 4.3 19.7 5.3 14.0 5.4 n.s. Organic Matter (%) 48.1 27.9 24.0 25.0 36.0 31.0 n.s. pH (water) 6.1 5.3 5.9 5.1 6.6 5.3 n.s. Soil Moisture (%) 55 38 63.5 40 23.5 46.0 n.s. Temperature (ºC) 14.8 12.1 14.8 13.9 16.8 15.1 n.s.

BT, bifurcated trees; DST, dead standing trees; MGBT, medium gap border trees; n.s. not significant (P≤0.05)

Microbial biomass and enzyme Moreover, DST ecological situation activities showed no significant differences (P>0.05) in FDA hydrolysis both ES and Epiphytes substrate in BT showed the SS. In contrast, MGBT ecological highest levels of FDA hydrolysis, MBC situation presented significant differences and MBN (Figure 2), the highest urease (P≤0.05) between SS and ES, with high activity (Figure 3) and significant values in SS. differences (P≤0.05) in respect to SS. All The MBC content showed significant results mentioned above are consistent differences (P≤0.05) in three evaluated with the high OM content, moisture and ecological situations, being higher in ES temperature (Table 1). (Figure 2b). The NBM showed significant

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differences (P≤0.05) in BT and MGBT -1

ecological situations (Figure 2c). h (A) Acid phosphatase activity presented -1 the highest levels in BT ecological situation (Figure 3a), probably to improve mol PNPg the low levels of available phosphorus μ (Table 2) with significant differences (P≤0.05) between SS and ES. -1 Finally, urease activity also showed h (B) -1 g the highest level in BT ecological 3 situation (Figure 3b), but in ES, with

significant differences (p ≤ 0.05) between mol NH both them. μ

-1

h Ecological situation -1 (A) Figure 3. Hydrolytic enzyme activities in epiphyte substrate (ES) and surrounding soil (SS) for three ecological situations in a

gfluorescein g gfluorescein temperate forest from south-central Chile. μ BT, bifurcated trees; DST, dead standing trees; MGBT, medium gap border trees. Acid phosphatase (A) and urease (B) -1 (B) activities.

mg C kg Correlations between biological variables

In general, close relationships were found among all evaluated biochemical (C) variables (Table 2). They were -1 significant (r = 0.60, P≤0.01), which agrees well with results reported by

mg N kg Alvear et al. (2008)

Ecological situation DISCUSSION

The selection of host species or

Figure 2. FDA hydrolysis (A), microbial phorophytes is consistent with the tree biomass carbon (MBC) (B) and nitrogen species best described as hosts by Zanetti (MBN) (C) in epiphyte substrate (ES) and (2004) and San Martín et al. (2008), who surrounding soil (SS) for three trees suggest that A. punctatum and N. obliqua ecological situations in a temperate forest tree species have special characteristics in from south-central Chile. BT, bifurcated their shaft and foliage that favour the trees; DST, dead standing trees; MGBT, colonization of vascular epiphytes. medium gap border. Moreover, all these species of epiphytes

132 Biochemical properties in vascular epiphytes, Reyes et al.

Table 2. Correlations among biochemical properties and physicochemical in both epiphytes substrate (ES) and surrounding soil forest land (SS) for three ecological situations in a temperate forest from south-central Chile.

Olsen FDA MBC MBN P-ase Urease pH OM Moist. Temp. P FDA 1 0.82 (**) 0.86 (**) n.s. 0.78 (**) n.s n.s n.s n.s. n.s. MBC 1 0.80 (**) n.s. 0.68 (**) 0.67 (**) n.s n.s n.s. n.s. MBN 1 n.s. 0.91 (**) n.s. n.s n.s n.s. n.s. P-ase 1 0.68 (**) n.s. 0.75 (**) 0.72 (**) n.s. n.s. Urease 1 n.s. n.s 0.96 (**) n.s. n.s. pH 1 n.s n.s. n.s. n.s. OM 1 n.s. n.s. n.s. Moist 1 n.s. n.s. Olsen P 1 n.s. Temp. 1 **Pearson correlation with a significance level 99% (P≤0.01). FDA = fluorescein diacetate hydrolysis, MBC = microbial biomass carbon, MBN = microbial biomass nitrogen, P-ase=acid phosphatase, Moist. = moisture, Temp. = temperature.

recorded in the sampling are preferably mainly those that were not fixed to the A. punctatum. This may be because this substrate. In addition, agreeing with tree species has denser and less Rousk and Nadkarni (2009), a possible translucent foliage, which reduces the explanation for the differences between light entering the forest, more specifically SS and ES in BT ecological situation is at its stem, which according to Godoy et related to OM content (Table 1). al. (1981) favours growth of epiphytic The high MBC content in ES is due ferns, with dominant composition in the primarily to the increased incorporation of region of temperate forest in Southern carbon compounds, proceeding from Chile (Godoy et al., 1989) fungi. The organism ability to retain and Thus, favoring higher rates of moisture immobilize them for later use as energy and temperature, and hence the activity of source; regarding the content of MBN, soil biota, which was reflected in BT Flores-Palacios and García-Franco ecological situation (Figure 2a). Besides, (2004), have indicated that the ES was covered with litter of tree species decomposition of biomass from vascular and shrubs creating a microclimate which and non-vascular epiphytes is rich in favored rapid degradation and nitrogen. It is consistent with the low C/N incorporation of material. This was biomass, increasing N input to the ES deposited on the bifurcation, which community and microorganisms, favoring increased the microorganism growth and the nutrient availability for their growth. enzyme secretion. We agree with On the SS, there was a greater Nadkarni et al. (2004), on to activity accumulation of plant material, but with a levels of active biota, they are dependent lower degradation rate, given a high C/N on the quantity and quality of compounds ratio soil biomass. It reduced energy from OM degradation, we can not foresee sources for microorganisms, not with that the degradation rate is maintained for respect to acid phosphatase activity, a period of time, even if there was a which was significantly higher (P≤0.05) mossy covered on the substrate, with (Figure 3a). This situation reflects a low abundant species of mosses and lichens, number and/or quality of phosphate

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substrates, but ES is not observed. plant material accumulated on the forest Furthermore, low P availability in SS soil, with a slow N release which led to a stimulated the secretion of phosphatase by rapid immobilization of nutrients by its own microorganisms and plant roots, microorganisms, while the P release which was helped by the extensive A. seems to be faster. Moreover, it punctatum root system. demonstrates a greater proliferation of Inselsbacher et al. (2007), suggested bacterial biomass of ES due to pH that epiphytes can be efficient in the condition (Table 1). + hydrolysis of urea to NH4 , urea excretion Acid phosphatase was significantly from insects that live along both the shaft higher in ES (Figure 3a, P≤0.05) due to and within the substrate; if urea content is the non-excretion of organic acids and rapidly hydrolyzed by the microorganisms phosphorus compounds from the roots of + when secreting urease, before the NH4 A. punctatum forest trees. This is caused ion, it can be assimilated by plants, which by differences in chemical plant material account for their microbial origin. In our composition produced in each study the urease activity was highly environment (data not shown) significant (P≤0.05) in ES. accumulated on the soil mostly leaves, The vegetation cover in ES in the DST branches, twigs and shaft residues, while ecological situation is formed by in ES with no material this Hymenophyllum species, especially quickly joined it. Urease activity showed Hymenophyllum plicatum Kaulf., some no significant differences (Figure 3b, mosses and lichens. Epiphytic species P>0.05), indicating that the contribution belonging to the Hymenophyllaceae of nitrogen compounds in two family are described as having a rhizome, environments was similar, varying the so each plant is connected to other of their reserve of this element by species for long stretches, even to the base microorganisms. of the tree shaft (Marticorena and The colonization of epiphytes in Rodríguez, 1995). This situation favors MGBT situation, preferably for the the regeneration of species in the species accounted for Hymenophyllum understory and interradicular tree space secundum Hook. Grev., which being no significant differences (P>0.05) demonstrated a high degree of in the hydrolysis of FDA between the ES desiccation, a sign of low humidity and and SS, even when the pH condition, substrate moisture. At the same time, moisture and temperature were more Benzing (1989) notes that favorable in the ES (Figure 2a). Hymenophyllaceae have a high resistance Furthermore, the accumulation of litter is to desiccation, being able to survive for mainly supplied from the N. obliqua, E. short periods, applying their strategy of cordifolia and A. punctatum species. This rolling and then returning to normal accumulation of litter stimulated the condition. This affected the activity levels proliferation and biota activity, generating of active biota (FDA hydrolysis), which an increase in OM degradation rate were significantly lower (P≤0.05) in ES. reaching a level similar to the substrate, The presence of a gap had a direct with a consequent release of carbon bearing on the shaft and so low moisture compounds and nitrogen for in ES and a lower OM accumulation and microorganisms, increasing their activity content was produced, limiting the release themselves. The high MBN content and transport of nutrients to and from indicates that the decomposition of lichen microorganisms. Linking the proliferation litter was lower than the decomposition of and activity of microorganisms in the

134 Biochemical properties in vascular epiphytes, Reyes et al. ecological condition, Arunachalam and situations, which is confirmed by the high Arunachalam, (2000) indicate that there correlation obtained (Table 2) finding the would be a strong correlation between the highest levels of microbial population in gap and the prevalence of bacterial BT and DST both ES and SS. Unlike biomass in both ES and SS since an MGBT, the gap effect on ES, had lower increasing community of denitrifying rates in both parameters due to lower bacteria is produced at higher pH values moisture levels, as the MBN is controlled (Table 1). However, MBN levels do not by soil moisture content (Hart and reflect this condition (Figure 2c). Firestone , 1991) (r = 0.88, P≤0.01). In Meanwhile, the MBC revealed no the case of MBC, it had a similar significant differences (P>0.05) due to interaction with the above mentioned, low plant material supply and/or substrate with high levels of correlation with the instability. The ecological strategy of FDA and MBN (r = 0.82 and r = 0.80, rolling of Hymenophyllaceae epiphytes respectively), although the MBC levels can act as insulation against of were always higher in epiphytic in three temperature and moisture fluctuations ecological situations. This suggests that inside the substrate avoiding greater FDA hydrolysis may be related to fungal carbon losses, solubilizing some biomass, according to Gaspar et al. (2001) carbonaceous components, but it is not and Anderson and Domsh (1980), since enough to increase levels of microbial higher moisture levels and more acid pH content to levels that differentiate them tend to proliferate these kinds of from the soil. However, they provide microorganisms (r = 0.63, P≤0.01 and r = and/or maintain a similar environment to 0.67, P≤0.01, respectively). the soil. Enzyme activities (Figure 3a and Acid phosphatase activity was 3b) were significantly higher (P≤0.05) in positively correlated to moisture and OM. SS, favored by the highest OM content, The composition of epiphytic species that accumulation and degradation and a more colonized the shafts affected the quality favorable condition of moisture and and solubility of phosphate compounds temperature. It is possible that different P that derived from the OM degradation (r = levels in each environment make a 0.75, P≤0.01, r = 0.72, P≤0.01, values for difference in the potential for acid OM and moisture, respectively). Urease phosphatase production by micro- activity presented correlation with FDA organisms, thus, a low P availability hydrolysis, MBC, MBN, moisture and stimulates the secretion of the enzyme. acid phosphatase activity. This situation Similarly, the secretion of urease derived appears to be related to the microbial from microorganisms actively transforms origin of the enzyme and the type of nitrogen compounds from the OM substrate, suggesting that urease is deposited on the substrate and from the affected by the nature of the vegetation bacterial biomass that grows on the leaves cover (Bastida et al., 2006; Steubing et of epiphytes, when pH and moisture al., 2002) conditions favor the proliferation of this type of microorganisms, it can fix significant nitrogen amounts. CONCLUSIONS

Correlations Our study demonstrated that each FDA hydrolysis and MBN properties situation presents a different microclimate showed very similar behavior in assessed for vascular epiphytes development,

135 R.C. Suelo Nutr. Veg. 10(2): 126 - 138 (2010)

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