SciELO - Scientific Electronic Library Online

vol.73 número4Increasing nitrogen rates in rice and its effect on plant nutrient composition and nitrogen apparent recoveryDynamics of soil water content during depletion cycles in peach orchards in a semiarid region índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados




Links relacionados


Chilean journal of agricultural research

versión On-line ISSN 0718-5839

Chilean J. Agric. Res. vol.73 no.4 Chillán dic. 2013 



Soil organic carbon storage and dynamics after C3-C4and C4-C3vegetation changes in sub-Andean landscapes of Colombia


Andrés F. Carvajal1*, Alexander Feijoo1, Heimar Quintero2, and Marco A. Rondón3

1Universidad Tecnológica de Pereira, Facultad de Ciencias Ambientales, Vereda La Julita, Pereira, Colombia.
*Corresponding author (

2Universidad Nacional de Colombia-Palmira Campus, Carrera 32 N° 12-00 Chapinero, Via Candelaria, Valle del Cauca, Colombia.
3International Development Research Centre (IDRC), 150 Kent Street, Ottawa, Ontario, Canada.

The soil C capture capacity and organic matter turnover rate vary according to photosynthetic pathways; therefore the evaluation of C at sites suffering changes from C3 to C4 vegetation and vice versa, is important to identify impacts of land use change on C cycle. This study aims to evaluate C storage under different land uses, and soil C dynamics using the 13C technique to identify the origin of soil C. In the Municipality of Alcala, Department of Valle del Cauca, Colombia, the natural abundance of δ13C was estimated, and data on land use history were gathered to calculate the organic matter turnover rate. The contribution of each type of vegetation to total percentage organic C and to storage at 0.30 m was estimated at sites suffering changes from C3 to C4 vegetation and vice versa. Average δ13C ranged between -25.79 and -20.72% at the three depths evaluated. Over a period of 13 yr, mature fallow lands replaced more than 70% of the C fixed by pastures over a period of 60 yr, whereas paddocks, over a period of 17 yr, only managed to replace 37.9% of the C fixed by associated coffee plantations during a period of 50-100 years. We conclude that the use of 13C avoided that C storage would have been attributed to current land uses when they are actually fixed by previous vegetation; and that C deposit from C3 vegetation is recalcitrant, while that corresponding to C4 vegetation has a relatively fast turnover rate.

Key words: Carbon stable isotope, 13C, land use change, organic matter, turnover rate.



Although it is estimated that 44% of the world's organic C is found in the first top meter of tropical soils (1500 Gt), the residency time of these deposits is shorter due to the combination of climatic factors and anthropogenic interventions that affect the entry of phytomass into the system as well as the thickness of the soil's protective porous layer (López-Ulloa et al., 2005; Tan and Lal, 2005).

Rates of C cycling are affected by the type, magnitude, severity, and frequency of anthropogenic interventions and, if the C cycle changes, they influence, in the long term, the isotopic signals that could serve as potential indicators to identify transformations in ecosystems according to change patterns generated by human disturbance (Boeckx et al., 2006). Estimates of C stocks and turnover rates are fundamental to understand the dynamics of terrestrial C. Furthermore, isotopic techniques are important because they can be applied in time scales that range from a few years to several hundreds of years (Oelbermann and Voroney, 2007).

The use of 13C allows C deposits derived from original vegetation to be differentiated from those of recent vegetation, provided that C3 plants predominate in one of these plant communities and C4 plants in the other (Lemma et al., 2006), thus serving as a valuable tool to confirm changes produced by the conversion of rainforests into paddocks (Lima et al., 2006).

Urban development and agriculture industrialization escalated during the second half of the 20th century in the Colombian Coffee Belt, located in the Andes. Starting in 1920, migrant farmers turned the slopes of this landscape into arable land and pastures and, as of 1940, sugarcane (Saccharum officinarum L.), cotton (Gossypium hirsutum L.), soybean (Glycine max (L.) Merr.), and maize (Zea mays L.) crops extended throughout the valleys, pushing livestock production toward the fragile volcanic slopes and intensifying the demand for land (Feijoo et al., 2007). In the La Vieja river watershed, where the municipality of Alcala is located, land use has changed significantly over the past 10 yr, triggered mainly by the coffee crisis. Traditional and modernized coffee crops were eradicated to plant plantain, citrus fruits, and pastures, mainly African star grass to produce meat and milk. The inappropriate management of intensive livestock production systems has had negative impacts on the environment such as deforestation, soil compaction and erosion, water contamination, loss of biodiversity, and changes in plant coverage and landscape (CRQ et al., 2008).

Based on the aforementioned changes, this study aims to evaluate soil C storage under different land uses and soil C dynamics, using the stable isotope technique (13C) to identify the origin of C at sites presenting changes in vegetation from C3 photosynthesis as coffee plantations (Coffea arabica L. var. Colombia) and mature fallow lands (Ocotea macropoda, Piper spp., Sauravia scabra, Trichanthera gigantea, Miconia aeruginosa) to C4 photosynthesis as pastures (Cynodon nlemfuensis Vanderyst) and sugarcane crops, and vice versa. The proposed hypothesis is that natural plant coverage such as mature fallow lands has a greater capacity to stabilize soil C than pastures, and that despite the fact that coffee crops have been replaced by pastures and sugarcane crops in the Municipality of Alcala, most of the C stored in the soil was fixed by C3 plants and it has been conserved even after 17 yr of change in land use.


Study site
The study was carried out in the Municipality of Alcala, located in the Department of Valle del Cauca, Colombia, at altitudes between 1150 and 1600 m a.s.l. This municipality is located on the western slope of the Central Cordillera (4°43'18.25" N, 75°51'22.91" W and 4°38'56.85" N, 75°42'11.94" W), an intermediate thermal floor (10002000 m a.s.l.) with an annual average temperature of 1824 °C, annual precipitation of 1350-2400 mm, relative humidity between 65-80%, and bimodal climate with two dry seasons (December-February and June-August) and two rainy seasons (March-May and September-November) (Alcaldia Municipal de Alcala, 2003).

Three altitudinal strata were defined: (1) between 1150 and 1300 m a.s.l.; (2) between 1301 and 1450 m; and (3) between 1451 and 1600 m. Two grids were constructed in each stratum, formed by 16 points projected every 200 m, for a total of 96 sampling sites. Grids 1 and 2 were located in the highlands of the La Cuchilla, El Congal, and Maravelez rural communities; grids 3 and 4 in the mid-altitude area of the La Polonia and Belgica rural communities; and grids 5 and 6 in the lowlands corresponding to the El Higuerdn rural community (Figure 1). Soils belong to two units of volcanic ash (Malabar and Chinchina) but differ in texture, base saturation, fertility, structure, and internal drainage (Table 1) (Alcaldia Municipal de Alcala, 2003; Cenicafé, 2007).

Figure 1. Location of sampling grids in three altitude zones of the Municipality of Alcala.

Table 1. Characteristics of the soils of the study area

Natural abundance of 13C
The natural abundance of 13C (δ13C), which is the ratio of 13C/12C based on international Vienna-Pee Dee Belemnite (V-PDB) standard (Peterson and Fry, 1987), was determined using the formula:

Samples were collected in the 0-10, 10-20, and 2030 cm depths using a metallic cylinder (98.12 cm3). Wet weight (W1) was recorded, soil samples dried, and the dry weight (W2) used to determine the bulk density (BD) with the formula: BD (g cm-3) = (W1-W2)/internal volume of cylinder. Carbon contents were calculated as follows:

Soil C (t ha-1) = %C x BD x T x A x 100

where, %C is percentage C, BD is bulk density (g cm-3), T is thickness of sampling layer (10 cm), A is area considered (1 ha).

At those sites where vegetation type changed from C3 photosynthesis (coffee plantations and mature fallow lands) to C4 photosynthesis (pastures and sugarcane crops) and vice versa, the contribution of each type of vegetation to the total percentage organic C was calculated using the formulas:

where Cc3 is C derived from C3 vegetation, Cc4 is C derived from C4 vegetation, δ13CSC3 is natural abundance of 13C measured in soil with C3 vegetation, δ13CSC4 is natural abundance of 13C measured in soil with C4 vegetation, δ13CVC3 is natural abundance of 13C in C3 vegetation (-26‰), δ13CVC4 is natural abundance of 13C in C4 vegetation (-12‰).

After calculating the contribution to the percentage total organic C, C storage fixed by each type of vegetation was estimated as follows:

Stored C derived from C3 vegetation (t ha-1) = %Cc3 x BD x D

Stored C derived from C4 vegetation (t ha-1) = %Cc4 x BD x D

where %Cc3 is percentage C derived from C3 vegetation, %Cc4 is percentage C derived from C4 vegetation, BD is bulk density (g cm-3), and D is sampling depth (cm).

Data analysis
Information on the land use history of each sampled field was gathered to identify changes over time and then calculate organic matter turnover rates (% yr-1), relating the δ13C to the establishment time of each system.

Nonparametric ANOVA-the Kuskal Wallis test for independent samples- was used to determine the natural abundance of 13C, using the SPSS program version 10.0 (SPSS, 1999). This allowed significant differences (p < 0.05) between sampling strata or areas, between sampling depths, and between land uses to be determined.


Variation of C with changes in land use and altitude above sea level
Altitude above sea level affects the organic carbon retained in the soil. The largest total storage of C (0-30 cm) were found in the highlands of Alcala (1450-1600 m a.s.l.), with values ranging between 102.67 and 123.64 t ha-1; in the mid-altitude area these values ranged between 43.08 and 105.40 t ha-1 and in the lowlands, between 41.75 and 92.33 t ha-1.

In terms of land use, the greatest accumulation of C occurred in plantain (137.97 t ha-1), coffee-banana-cassava (134.90 t ha-1), and giant bamboo (130.43 t ha-1) in the upland area; mature fallow land (43.08 t ha-1) in the mid-altitude area; and giant bamboo-cacao (41.75 t ha-1) in the lowlands. Soils, despite having the same land use, modified the amount of C fixed depending on the altitude. Considerable reductions were recorded. For example, a difference of 59.59 t ha-1 accumulated C was observed between mature fallow land in the highlands and mature fallow land in the lowlands. This trend was also observed in the other land uses present in the evaluated strata. The lowest amounts of accumulated C occurred in the altitudinal range of 1150-1300 m a.s.l. (Table 2).

Table 2. Average storage of C according to land use in upper 0-30 cm of soil.

SD: Standard deviation.

On the other hand, altitude above sea level did not affect the natural abundance of 13C, presenting a low correlation coefficient (-0.2) and absence differences (p < 0.05) between sampling areas. The average values of abundance of this isotope ranged between -25.18 and -21.72‰ for all uses evaluated. None of obtained values were similar to those of tropical pastures (-12‰ on average), emphasizing the predominance of C3 plants in C fixation in the soil.

Organic matter turnover rates
Of the 96 sampled sites, 27 presented changes from C3 to C4 vegetation and vice versa. The regrowth of vegetation was allowed at three upland sites that had been used as paddocks over a 60-yr period; the land transformed into mature fallow lands after 13 yr. Sugarcane crops that had been established for 2 yr were found at three lowland sites that had previously been planted to coffee. The remaining 21 samplings were performed in pastures, 1 to 17 yr old that have previously been planted to coffee.

The δ13C of sites that had undergone a change in vegetation ranged between -25.31 and -18.82‰ for the depth of 0-10 cm; between -25.00 and -21.21‰ for the depth of 10-20 cm; and between -25.42 and -20.05‰ for the depth of 20-30 cm. Pastures and sugarcane crops conserved the C from the coffee plantations, whereas the mature fallow lands with δ13C values close to those of C3 vegetation (-26‰ on average) showed that, within a 13-yr period, they managed to replace the C derived from pastures over a 60-yr period.

The turnover rates of organic C in the soil at the three depths ranged between 0.3-20.9% yr-1. The rapidness with which pastures stabilized C was evidenced in the three 1-yr pastures and in the three 2-yr sugarcane crops, decreasing over time until a minimal rate was found in the 17-yr-old pasture (Pa19).

The highest turnover rates were recorded in Pa3 at depths of 10-20 and 20-30 cm (20.1 and 19.3% yr-1, respectively), attributable to root system architecture. High turnover rates were also observed at the three depths of several sugarcane samplings (Cn1, Cn2), presenting values of 16.5 and 16.2% yr-1 at 0-10 cm, 14.4 and 11.9% yr-1 at 10-20 cm, and 13.9 and 11.5% yr-1 at 20-30 cm (Table 3).

Table 3. Organic matter turnover rates at sites with changes in vegetation
from C3 photosynthesis to C4 photosynthesis or vice versa.

At seven sites corresponding to mature fallow land (Mfl1), cut-and-carry grass (Ccg) and pastures (Pa1, Pa4, Pa6, Pa7), the natural abundance of 13C tended to increase with depth (less negative values), as well as the organic matter turnover rates, contrary to other mature fallow lands (Mfl3, Mfl4), pastures (Pa10, Pa15, Pa16, Pa17) and sugarcane (Cn2, Cn3).

Origin of soil organic carbon
In mature fallow land, the total average % C ranged between 5.57 and 6.81%, and the highest proportion was derived from C3 vegetation. Of the four sites evaluated, Mfl3 presented the highest percentage of C derived from C4 vegetation (26.8%). Two more sites (Mfl1 and Mfl2), despite being geographically close and presenting similar land use histories, differed in the amount of C contributed by the vegetation, mainly because the turnover rates in Mfl3, at all three depths, were lower than those of the other three mature fallow lands.

Total C storage in fallow land ranged between 93.26 and 118.02 t ha-1, the highest value corresponding to Mfl4 where 104.17 t ha-1 were derived from C3 vegetation and only 13.85 t ha-1 from C4 vegetation (Figure 2). A predominance of C fixed by C3 plants, which ranged between 62 and 91.7%, was observed at sites where grasses were present. At sites presenting pastures in which vegetation changes had occurred over a period of 1 to 7 yr, the percentage of total C tended to be higher, decreasing with increasing time of establishment. The storage of C was higher in Pa7, where 101.57 t ha-1 were derived from previously existing coffee crops and only 20.31 t ha-1 from pastures with 7 yr of establishment (Figure 3).

Figure 2. Origin and storage of C (0-30 cm) at sites presenting changes from
C4 vegetation to C3 vegetation. Mfl: Mature fallow land.

Figure 3. Origin and storage of C (0-30 cm) at sites presenting changes from C3 vegetation to
C4 vegetation. Ccg: Cut-and-carry grass, Pa: pasture, Cn: sugarcane.


The estimation of soil C storage was complemented with the calculation of organic matter turnover rates, because according to Solomon et al. (2002) and Desjardins et al. (2006), the change in land use alters the speed at which the organic molecules oxidized, therefore affecting its accumulation and mineralization. Oelbermann and Voroney (2007) assert that those turnover rates are key to understanding the dynamics of terrestrial carbon and may even allow the C flow between soil and atmosphere to be calculated at a given moment. Therefore the 13C technique is increasingly important in studies on soil C because it allows different time scales, which can range from 1 to several hundreds of years, to be evaluated (Bernoux et al., 1998). In the case of this study, the rates at sites with different land use histories, where changes of vegetation occurred over a period from 1 to 17 yr, were calculated. In addition, the use of stable C isotopes was a tool that prevented erroneous conclusions being made about the sites that had undergone changes in vegetation. If the evaluation had only taken into account the results obtained with the dry combustion method, then C storage would have been attributed to current land uses when they are actually product of the C fixed by previous vegetation.

Although tropical pastures contain C3 grasses that make considerable contributions to isotopic signals, this study as well as that conducted by López-Ulloa et al. (2005) assumed that the highest contribution came from grasses, indicating the usefulness of identifying the C contributed by the pasture and evaluating the capacity of C4 plants to stabilize and fix C.

Diels et al. (2001), on the other hand, recognize that the use of the technique to determine the natural abundance of 13C has been limited to situations presenting an abrupt transition of C3 vegetation to C4 vegetation or vice versa. When combined with models to determine soil organic C such as CENTURY (Parton et al., 1987) or ROTHC (Jenkinson et al., 1992), the signals of this isotope could potentially be used to forecast changes in more complex situations where no drastic changes have occurred or in systems where both two types of vegetation are found mixed together.

At 24 of the 96 sites that were sampled, the type of photosynthesis of the vegetation changed when coffee plantations were replaced with pastures or sugarcane. The organic matter at these sites had not yet been stabilized because signals of 13C fixed by previous vegetation were found. This is why it is important to relate the estimation of the natural abundance of 13C with the farmers' knowledge of transformations in land use at each sampling site so as not to overestimate capacity of grasses to capture C.

The 13C values in the three sampling areas were less negative at the depth of 20-30 cm; however, in relation to land use, the 13C did not increase with depth in seven of them, whereas this trend was maintained in the remaining 11. Coffee-plantain, coffee under shade, and fruit trees presented differences (p < 0.05) in 13C values between the depths of 0-10 and 20-30 cm, with variations above 1 unit (‰). The findings of Sisti et al. (2004) agree with the above results and indicate that soil organic matter at deeper depths has a higher humus content, which explains the higher 13C values with increasing depth in the soil profile. Differences between 1 and 2 units (‰) are found between the surface layer and 100-cm depth. In this study, however, changes of this magnitude were also found between the surface layer and 30-cm depth. The same authors put forward that the factors responsible for these increases with depth could be related to the increased use of fossil fuels with low abundance of 13C over the past 150 yr, decreasing by at least 1.3% the average 13C in the atmosphere. Furthermore, soil organic matter is increasingly older with increasing depth, so it is possible that the C previously introduced into the soil via photosynthesis has higher 13C values. Rao et al. (1994) indicate that another possible cause of this phenomenon could be the preferential decomposition in deeper soil layers, with components or molecules with low 13C values being removed first.

Sites with pastures that are 9, 10, and 17-yr old yielded 13C values that varied between -18.82 and -25.16‰ at the three depths, showing a predominance of C from coffee plantations (C3). In an area with predominance of Oxisols and an average temperature of 26 °C (Carimagua, Colombia), Rao et al. (1994) found, on the contrary, that 12-yr-old pastures that presented a quick organic matter turnover rate with 13C values ranging between -12.08 and -13.26‰, indicating that the C in these soils had been derived from pastures (C4). The foregoing shows that soil type and temperature could affect the increase in organic matter turnover rate, indicating a regional effect on C dynamics and, as a result, greater susceptibility of soil C to land use changes in a given area.

Manfrinato et al. (2001) conducted a study on native tropical rainforest, a 20-yr-old pasture, and pastures that had been abandoned for 5 or 10 yr and found 13C values of -27.74, -22.90, -25.10, and -26.49‰, respectively, at a depth of 0-10 cm. Results indicated the following: the area under native vegetation presented the highest values corresponding to C3 vegetation; 13C value of the 20-yr-old pasture had still not reached the values of C4 vegetation (on average 14‰); and abandoned pasture colonized by shrub and tree vegetation tended to present more negative values similar to those of initial vegetation. Turnover rates in these areas were lower than those found in Alcala, where pastures 9 and 10 yr old presented values of -19.90‰ (Pa8-lowlands), with an organic matter turnover rate of 4.3% yr-1.

All sites were observed to have a high capacity to stabilize organic matter, contrary to that reported in sandy soils of South Africa, where soils have little potential for stabilization of organic matter (Lobe et al., 2005). In this study, in abandoned pastures presenting successive tree vegetation, 13C values at all depths after 13 yr ranged between -20.64 and 25.42%, being closer to the average of C3 vegetation (-26%) than to that of C4 vegetation (-14%). Outliers were found at lowland sites Pa11 (0.3% yr-1) and Pa13 (1.0% yr-1). These values were lower than those found by Roscoe et al. (2001) in Brazil where pastures, 23 years after establishment, had only managed to replace 36% C from native vegetation, indicating a turnover rate of 1.6% yr-1, which is regarded as fast and notably differs from rates found at sites such as Cn29 and Cn30, where transformation occurred at a rate 16.5 and 16.2% yr-1, respectively.

The high percentage of C derived from C3 plants at sites with pastures of several years, compared with that of fallow land in highlands with little C from C4 plants, indicates that the C deposit from C3 vegetation is recalcitrant, while that corresponding to C4 vegetation has a relatively fast rate of return (Lemenih et al., 2005; Liao et al., 2006).

Michelsen et al. (2004) in Ethiopia as well as Krull and Skjemstad (2003) and Wynn et al. (2005) in Australia found that the abundance of 13C increased —in other words, presented negative less values— from the surface downward to the deepest soil layers. These findings are consistent with the isotope theory that states that respiratory losses of isotopically-light C during decomposition cause that, with depth, the residual C (in other words, the oldest) is enriched with isotopes. The increase in 13C in the lower layers also indicates the preferential loss of 12C molecules through kinetic fractionation during biological transformation (Krull et al., 2006).

In the Brazilian Amazon region, Desjardins et al. (2004) found 13C values ranging between -28.9 and -27.3‰ in natural forests; -28.0 and -25.8‰ in 4-yr-old pastures; -25.9 and -22.2 in 8-yr-old pastures; and -24.4 and -20.3‰ in 15-yr-old pastures. These results show the effect of pastures on the isotope over time. In Costa Rica, Oelbermann et al. (2006) conducted studies in both agro-forestry systems and monocultures, finding that fertilizer application or use of N-fixing plants as plant cover did not directly affect C turnover rates in the soil. Therefore the application of the 13C technique indicated that changes in isotopic signals were directly related to the type of vegetation contributing plant residues to the soil surface.


The use of stable C isotopes was a tool that prevented erroneous conclusions being made about the sites that had undergone changes in vegetation. If the evaluation had only taken into account the results obtained with the dry combustion method, then C storage would have been attributed to current land uses when they are actually product of the C fixed by previous vegetation. Besides, we conclude that the knowledge of transformations in land use at each sampling site was a key factor to prevent overestimating the capacity of grasses to capture C.

In general, the soils of the Municipality of Alcala have relatively fast turnover rates, showing a high capacity to stabilize organic matter, especially at sites where pastures were abandoned. On the other hand, the natural abundance of 13C was a chemical property of the soil that was related to the predominant type of vegetation at sampling sites and not to biophysical factors, such as altitude above sea level. The values of this isotope increased with soil depth due to the age of the organic matter and to selective decomposition processes in which isotopically light C is degraded first.

Mature fallow lands were found to have a greater capacity to stabilize high C stabilization capacity, because within a period of 13 yr, these soils could replace more than 70% of the C that had been fixed by pastures over a 60-yr period; while the maximum C that these latter pastures could replace in periods of establishment up to 17 yr was 37.9% of the C fixed by coffee plantations over periods of 50-100 yr.

The last shows the importance of C3 vegetation on C cycle, because it fixes great quantities of soil C and potentiates its storage during long periods. Therefore we conclude that C deposit from C3 vegetation is recalcitrant, while that corresponding to C4 vegetation has a relatively fast turnover rate.


The authors thank the Universidad Tecnológica de Pereira, Colombia's Administrative Department of Science, Technology and Innovation (Colciencias) and the Genetic Resources and Biodiversity Research and Studies Center (CIEBREG). Our sincere appreciation also goes to all members of the Tropical Andean Agroecosystems Management (GATA) group for their support throughout this study, to the International Center for Tropical Agriculture (CIAT) for helping with sample analyses, and to the farm owners and managers of the 48 landholdings where samples were taken for allowing us to study their production systems.


Alcaldia Municipal de Alcala. 2003. Esquema de ordenamiento territorial-diagnóstico Año 2003-2011. Secretaria de Planeación, Alcala, Valle del Cauca, Colombia.         [ Links ]

Bernoux, M., C.C. Cerri, C. Neill, and J.F.L. de Moraes. 1998. The use of stable carbon isotopes for estimating soil organic matter turnover rates. Geoderma 82:43-58.         [ Links ]

Boeckx, P., M. Van Meirvenne, F. Raulo, and O. Van Cleemput. 2006. Spatial patterns of δ13C and δ15N in the urban topsoil of Gent, Belgium. Organic Geochemistry 37:1383-1393.         [ Links ]

Cenicafé. 2007. Unidades de suelos. Centro Nacional de Investigaciones de Café (Cenicafé), Manizales, Colombia. Available at (accessed September 2011).         [ Links ]

CRQ, CARDER, CVC, UAESPNN, IDEAM, MAVDT, GTZ. 2008. Plan de ordenación y manejo de la cuenca del rio La Vieja. Corporación Autónoma Regional del Quindio (CRQ), Corporación Autónoma Regional de Risaralda (CARDER), Corporación Autónoma Regional del Valle del Cauca (CVC), Unidad Administrativa Especial del Sistema de Parques Nacionales Naturales (UAESPNN), Instituto de hidrologia, meteorologia y estudios ambientales (IDEAM), Ministerio de Ambiente, Vivienda y Desarrollo Territorial (MAVDT), Agencia de Cooperación Alemana (GTZ), Armenia, Colombia. Available at ORDENACION%20Y%20MANEJO%20RIO%20LA%20 VIEJA.pdf (accessed July 2011).         [ Links ]

Desjardins, T., E. Barros, M. Sarrazin, C. Girardin, and A. Mariotti. 2004. Effects of forest conversion to pasture on soil carbon content and dynamics in Brazilian Amazonia. Agriculture, Ecosystems & Environment 103:365-373.         [ Links ]

Desjardins, T., P.J. Folgarait, A. Pando-Bahuonc, C. Girardind, and P. Lavelle. 2006. Soil organic matter dynamics along a rice chronosequence in north-eastern Argentina: Evidence from natural 13C abundance and particle size fractionation. Soil Biology and Biochemistry 38:2753-2761.         [ Links ]

Diels, J., B. Vanlauwe, N. Sanginga, E. Coolen, and R. Merckx. 2001. Temporal variations in plant δ13C values and implications for using the 13C technique in long-term soil organic matter studies. Soil Biology and Biochemistry 33:1245-1251.         [ Links ]

Feijoo, A., M.C. Zuñiga, H. Quintero, y P Lavelle. 2007. Relaciones entre el uso de la tierra y las comunidades de lombrices en la cuenca del rio La Vieja, Colombia. Pastos y Forrajes 30:235-249.         [ Links ]

Jenkinson, D.S., D.D. Harkness, E.D. Vance, D.E. Adams, and A.F. Harrison. 1992. Calculating net primary production and annual input of organic matter to soil from the amount and radiocarbon content of soil organic matter. Soil Biology and Biochemistry 24:295-308.         [ Links ]

Krull, E.S., E.A. Bestland, J.O. Skjemstad, and J.F. Parr. 2006. Geochemistry (δ13C, δ15N, 13C NMR) and residence times (14C and OSL) of soil organic matter from red-brown earths of South Australia: Implications for soil genesis. Geoderma 132:344-360.         [ Links ]

Krull, E.S., and J.O. Skjemstad. 2003. δ13C and δ15N profiles in 14C-dated Oxisol and Vertisols as a function of soil chemistry and mineralogy. Geoderma 112:1-29.         [ Links ]

Lemenih, M., E. Karltun, and M. Olsson. 2005. Soil organic matter dynamics after deforestation along a farm field chronosequence in southern highlands of Ethiopia. Agriculture, Ecosystems and Environment 109:9-19.         [ Links ]

Lemma, B., D.B. Kleja, I. Nilsson, and M. Olsson. 2006. Soil carbon sequestration under different exotic tree species in the southwestern highlands of Ethiopia. Geoderma 136:886-898.         [ Links ]

Liao, J.D., T.W. Boutton, and J.D. Jastrow. 2006. Organic matter turnover in soil physical fractions following woody plant invasion of grassland: Evidence from natural 13C and 15N. Soil Biology and Biochemistry 38:3197-3210.         [ Links ]

Lima, A.M.N., I.R. Silva, J.C.L. Neves, R.F. Novais, N.F. Barros, E.S. Mendoça, et al. 2006. Soil organic carbon dynamics following afforestation of degraded pastures with eucalyptus in southeastern Brazil. Forest Ecology and Management 235:219-231.         [ Links ]

Lobe, I., R. Bol, B. Ludwig, C.C. Du Preez, and W. Amelung. 2005. Savanna-derived organic matter remaining in arable soils of the South African Highveld long-term mixed cropping: Evidence from 13C and 15N natural abundance. Soil Biology and Biochemistry 37:1898-1909.         [ Links ]

López-Ulloa, M., E. Veldkamp, and G.H.J. de Koning. 2005. Soil carbon stabilization in converted tropical pastures and forests depends on soil type. Soil Science Society of America Journal 69:1110-1117.         [ Links ]

Manfrinato, W., M.C. Piccolo, C.C. Cerri, M. Bernoux, y C.E. Pellegrino. 2001. Medición de la variabilidad espacial y temporal del carbono del suelo con el uso de isdtopos estables, en una transición bosque-pradera en el estado de Parana, Brasil. p. 1-17. Simposio Internacional Medición y Monitoreo de la Captura de Carbono en Ecosistemas Forestales, Valdivia, Chile. 19-20 Octubre. Universidad Austral de Chile, Facultad de Ciencias Forestales, Valdivia, Chile.         [ Links ]

Michelsen, A., M. Andersson, M. Jensen, A. Kj0ller, and M. Gashew. 2004. Carbon stocks, soil respiration and microbial biomass in fire-prone tropical grassland, woodland and forest ecosystems. Soil Biology and Biochemistry 36:1707-1717.         [ Links ]

Oelbermann, M., and R.P. Voroney. 2007. Carbon and nitrogen in a temperate agroforestry system: using stable isotopes as a tool to understand soil dynamics. Ecological Engineering 29:342-349.         [ Links ]

Oelbermann, M., R.P. Voroney, D.C.L. Kass, and A.M. Schlonvoigt. 2006. Soil carbon and nitrogen dynamics using stable isotopes in 19- and 10-year-old tropical agroforestry systems. Geoderma 130:356-367.         [ Links ]

Parton, W.J., D.S. Schimel, C.V. Cole, and D.S. Ojima. 1987. Analysis of factors controlling soil organic matter levels in Great Plains grasslands. Soil Science Society of America Journal 51:1173-1179.         [ Links ]

Peterson, B.J., and B. Fry. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology, Evolution, and Systematics 18:293-320.         [ Links ]

Rao, I.M., M.A. Ayarza, and R.J. Thomas. 1994. The use of carbon isotope ratios to evaluate legume contribution to soil enhancement in tropical pastures. Plant and Soil 162:177-182.         [ Links ]

Roscoe, R., P. Buurman, E.J. Velthorst, and C.A. Vasconcellos. 2001. Soil organic matter dynamics in density and particle size fractions as revealed by the 13C/12C isotopic ratio in a Cerrado's Oxisol. Geoderma 104:185-202.         [ Links ]

Sisti, C.P.J., H.P. dos Santos, R. Kohhann, B.J.R. Alves, S. Urquiaga, and R.M. Boddey. 2004. Change in carbon and nitrogen stocks in soil under 13 years of conventional or zero tillage in southern Brazil. Soil and Tillage Research 76:39-58.         [ Links ]

Solomon, D., F. Fritzsche, J. Lehmann, M. Tekalign, and W. Zech. 2002. Soil organic matter dynamics in the subhumid agroecosystems of the Ethiopian highlands: evidence from natural C-13 abundance and particle-size fractionation. Soil Science Society of America Journal 66:969-978.         [ Links ]

SPSS. 1999. SPSS Base 10.0 Applications Guide. SPSS Inc., Chicago, Illinois, USA.         [ Links ]

Tan, Z., and R. Lal. 2005. Carbon sequestration potential estimates with changes in land use and tillage practice in Ohio, USA. Agriculture, Ecosystems and Environment 111:140-152.         [ Links ]

Wynn, J.G., M.I. Bird, and V.N.L. Wong. 2005. Rayleigh distillation and the depth profile of 13C/12C ratios of soil organic carbon from soils of disparate texture in Iron Range National Park, Far North Queensland, Australia. Geochimica et Cosmochimica Acta 69:1961-1973.         [ Links ]

Received: 5 December 2012.
Accepted: 4 September 2013.

Creative Commons License Todo el contenido de esta revista, excepto dónde está identificado, está bajo una Licencia Creative Commons