Applied Soil Ecology 29 (2005) 282–289 www.elsevier.com/locate/apsoil
Soil C and N dynamics in primary and secondary seasonally dry tropical forests in Mexico Vinisa Saynes a, Claudia Hidalgo b, Jorge D. Etchevers b, Julio E. Campo a,* a
Instituto de Ecologı´a, Universidad Nacional Auto´noma de Me´xico, AP 70-275, 04510 Mexico, DF, Mexico b Instituto de Recursos Naturales, Colegio de Postgraduados, 56230 Montecillo, Mex., Mexico Received 6 July 2004; accepted 22 November 2004
Abstract The nature and size of soil carbon (C) and nitrogen (N) pools and turnover were compared in secondary and primary forests in a seasonally dry tropical region of Mexico. Total soil C and N, microbial biomass C and N, mineral (ammonium and nitrate) N pools and potential mineralization and nitrification were measured in samples collected during the dry and rainy seasons in early-, mid-, late-successional and primary forests. We hypothesized that the previous agricultural land use of secondary forests would result in lower soil C and N stocks than in primary forest soils, as well as in the seasonal dynamics changes of these two elements. The expected pattern of decreasing soil C and N after a previous agricultural land use did not occur. Soil C was unaffected by the successional stage of the forest. In addition, early- and mid-successional forests registered the highest total and mineral N pools and potential N transformations, whereas primary forests had the lowest N pools and potential cycling. The total soil C and N pools did not change with the sampling season. However, the nitrate pool decreased at the beginning of the rainy season in all forest soils, as did the ammonium pool in primary forests. A striking contrast of the effects of the rainfall (i.e., dry season versus rainy season) seasonality on the microbial biomass and its C:N ratio was observed among forests; latesuccessional and primary forests recorded the lowest values of both parameters at the beginning of the rainy season, whereas early- and mid-successional forests showed the highest values at this sampling date. Therefore, potential N transformations in all forests were the highest during the rainy season. Our study on the consequences of the land cover change on soils, following the discontinuation of agricultural practices, allows us to conclude that the nutrient dynamics in this ecosystem will vary depending on the successional stage of the forests. This work suggests that the full restoration of soil C and N dynamics will take ca. 60 years of secondary succession. # 2005 Elsevier B.V. All rights reserved. Keywords: Potential nitrogen transformation; Soil microbial carbon; Soil microbial nitrogen; Tropical soils
1. Introduction * Corresponding author. Tel.: +52 55 5622 9027; fax: +52 55 5616 1976. E-mail address:
[email protected] (J.E. Campo).
Primary forests in seasonally dry tropical regions have undergone intense land use change, ranging from widespread shifting cultivation agriculture to land
0929-1393/$ – see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.apsoil.2004.11.007
V. Saynes et al. / Applied Soil Ecology 29 (2005) 282–289
clearing for intensive agriculture and selective logging. These land uses alter the structure and function of forested lands producing a mosaic of secondary forests of different ages and often generate new feedbacks in terms of subsequent human use. Consequently, a major goal in assessing environmental change is to understand how biogeochemical processes respond to land use change, emphasizing the potential of a man-dominated landscape to sustain continuous human use. Secondary forests are usually fast-growing ecosystems. However, their successful management and forest regeneration plans require from us to know how well the nutrient cycling, soil conditions and fertility recover following the discontinuation of agricultural practices. An extensive exploration of the factors regulating the nutrient dynamics of tropical seasonal forests has been carried out, in particular the role of the microbial biomass in the availability of nutrients for trees (Singh et al., 1989; Campo et al., 1998). Variations in soil microclimatic conditions affect the microbial activity and biomass and subsequently the overall carbon and nitrogen cycling (Paul and Clark, 1996). As soil moisture availability plays a significant role in microbial activity and nutrient cycling dynamics in tropical seasonal ecosystems (Lodge et al., 1994), it probably represents a significant factor in the regeneration of forest vegetation and functioning of the ecosystem. The relationship between seasonal rainfall levels, the microbial biomass and nutrient cycles in unperturbed seasonal forests is well established (see Eaton, 2001), however such association has not been studied in secondary forest successions where significant changes in composition and density of forest vegetation take place. Studies on the soil microbial biomass, a sink and source of plant nutrients in tropical forests, have not attracted the attention of foresters and soil scientists. However, to understand the relationships between the microbial biomass, soil moisture and nutrient cycles in tropical forest ecosystems has important implications for soil and forest management practices. The present study was designed: (1) to determine the effects of forest age on microbial biomass C and N, the pools of total soil C and N and potential N transformations and (2) to evaluate the effects of rainfall seasonality on the soil and microbial nutrient
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dynamics in primary and secondary tropical seasonal forests. We measured the seasonal soil microbial biomass C and N (during the dry season, and at the beginning and in the middle of the rainy season), the standing pools of total soil C and N and the potential N transformations in sites of replicate chronosequence of forest succession in the center of Mexico. We expected soil C and N pools to be lower in the early stages of forest succession and increase with forest age. Finally, we expected a decrease of the soil microbial biomass and nutrients at the beginning of the rainy season in both primary and secondary forests.
2. Methods 2.1. Study areas Over the last 40 years, land use in Morelos, center of Mexico, has changed from primary tropical seasonal forest to agricultural use (Trejo and Dirzo, 2000). This shift has reduced the land forest area and created a mosaic of agricultural areas and secondary forests of different ages. The abundance of successional forest covers offers an opportunity to examine the effects of land cover change and forest recovery on the microbial biomass, soil C and potential rates of N cycling. The study was conducted in a primary tropical forest area and three secondary tropical forest areas, adjacent to the Sierra de Huatla Reserve region (188280 N, 998010 W). The native vegetation in this region is made up of seasonally dry tropical forest and Leguminosae, which is the most important family (Dorado, 1997). Long-term climatic data from weather stations show that the region is characterized by a distinct period of low precipitation (Garcı´a, 1988). The climate in the area is hot and sub-humid. Average monthly temperatures are high (24.5 8C) and vary little, ranging from 22.8 to 26.2 8C. Mean annual precipitation is 851 mm (Comisio´ n Nacional del Agua, personal communication), most of which falls between June and October (90% of total annual). The region is characterized by steep mountain terrain. Soils derived from underlying granites are classified as Entisols (Dorado, 1997). In a continuous mosaic of primary and secondary tropical seasonal forests, we selected four areas of
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Table 1 Site characteristics for different seasonally dry tropical forests studied at Sierra de Huatla, Mexico Forest
Time current recovery of forest (year) Basal areaa (m2 ha1) Tree densitya (ind ha1) Tree heighta (m) Litterfall productionb (g m2 per year) Litterfall Nb (g m2 per year)
Primary
Early-successional
Mid-successional
Late-successional
16.5 (1.4) 2153 (377) 7.8 (0.7) 417 (48) 6.32 (0.52)
10–15 8.5 (1.1) 2049 (293) 4.1 (0.5) 588 (28) 9.14 (0.40)
20–30 9.7 (1.0) 1938 (322) 5.7 (0.6) 562 (23) 7.84 (0.25)
60 12.8 (1.2) 2023 (215) 5.9 (0.5) 377 (45) 6.00 (0.47)
Data are means (standard error). a For all trees at least 2.5 cm in diameter at the start of the study. b Litterfall production and its N content data between 2001 and 2002 provided courtesy of P. Valdespino.
primary forest, and four of each, early-successional (10–15-year-old), mid-successional (20–30-year-old) and late-successional (60-year-old) forests. All forest areas were 2 km away from each other. In the region most of the forest had been converted to maize (or milpa) cultivation by slash-and-burn. In June and July 2001, a 12 m 12 m plot was established in each forest area and every tree of 2.5 cm or larger in diameter at breast height (1.3 m aboveground) was measured and identified. The primary forest had the largest basal area (Table 1). Among secondary forests, basal area increases along a series from early- through mid-successional to late-successional forests. Aboveground litterfall production and associated N flux are higher in early- and mid-successional forests than in late-successional and primary forests. Soils are shallow ( 0.05). The successional stage did not have a significant effect on microbial biomass N, except during the dry season when soils from early-successional forests had larger pools than those from primary forests. As was the case for the microbial biomass C pool, the microbial C:N ratio differed considerably among forests. The corresponding ANOVA indicated that this difference is significant (P < 0.05) and paired comparisons using the Tukey–Kramer HSD test shows that soils from mid-successional forests had consistently the highest C:N ratios. The microbial C mean contribution to soil C (measured as the ratio between the C pools in microbial biomass and total C pools in soils) ranged from 1.2 to
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Table 2 Pools of total soil C and N and microbial biomass C and N for different seasonally dry tropical forests studied at Sierra de Huatla, Mexico Forest Primary
Early-successional
Mid-successional
Late-successional
Total soil C (g m ) Dry season Rainy season (beginning) Rainy season (midway)
3403 (465)a1 3594 (732)a1 3827 (665)a1
4093 (330)a1 3786 (721)a1 3671 (890)a1
4531 (208)a1 3169 (394)a1 4110 (543)a1
3809 (394)a1 3985 (471)a1 4358 (626)a1
Total soil N (g m2) Dry season Rainy season (beginning) Rainy season (midway)
92 (29)b1 154 (27)a1 141 (31)b1
201 (8)a1 225 (33)a1 215 (24)a1
238 (20)a1 216 (38)a1 223 (13)a1
183 (18)b1 253 (53)ab1 184 (19)ab1
2
C:N Dry season Rainy season (beginning) Rainy season (midway)
37.2 (7.3)a1 23.3 (1.9)a1 27.1 (2.1)a1
19.6 (1.5)b1 16.8 (2.5)b1 17.3 (3.9)b1
17.5 (1.5)b1 14.7 (2.3)b1 18.4 (2.3)b1
20.2 (2.0)b1 17.9 (1.9)b1 23.6 (3.9)ab1
Soil microbial biomass Microbial C (g m2) Dry season Rainy season (beginning) Rainy season (midway)
63.0 (9.3)ab1 17.7 (5.2)b2 46.2 (4.9)a1
41.6 (9.0)b2 83.8 (11.8)a1 30.6 (8.5)a2
72.7 (6.3)a1 81.6 (4.1)a1 53.4 (8.1)a2
70.2 (8.3)a1 21.0 (5.0)b2 47.2 (5.5)a1
Microbial N (g m2) Dry season Rainy season (beginning) Rainy season (midway)
5.4 (0.6)b1 4.6 (0.3)a12 4.0 (0.3)a2
7.4 (0.7)a1 4.5 (0.1)a2 5.1 (0.8)a2
Microbial C:N Dry season Rainy season (beginning) Rainy season (midway)
11.7 (2.3)a1 3.8 (1.2)b2 11.6 (1.0)a1
5.6 (1.9)b2 18.6 (1.8)a1 6.0 (1.6)b2
5.8 (0.8)ab1 4.0 (0.3)a2 4.6 (0.2)a12 12.5 (2.0)a2 20.4 (2.6)a1 11.6 (3.5)a2
6.3 (0.3)ab1 4.1 (0.4)a2 3.1 (0.1)a3 11.2 (2.6)ab1 5.1 (1.1)b2 15.2 (0.9)a1
Data are means (standard error). Different letters (a, b, c) indicate means are significantly different (P < 0.05), when testing for differences among forest within each time period. Different numerals (1, 2, 3) indicate means are significantly different (P < 0.05), when testing for changes through time within a forest.
1.8%. This mean contribution was the highest in midsuccessional forest sites and the lowest in primary forest sites. In contrast, the contribution of microbial N to total soil N was the lowest in mid-successional forests (1.7%) and increased following the order late-successional < early-successional < primary forest (ranged between 1.9 and 2.5%). The microbial biomass C pool in soils differed considerably among the three sampling dates according to the successional stage (Table 2). Soils from latesuccessional and primary forests had a microbial biomass C pool three times larger, when determined in the dry season than at the beginning of the rainy season (P < 0.01). In contrast, early- and mid-successional forest soils had the largest pools of microbial biomass C at the beginning of the rainy season, and the lowest pools were detected in the middle of this season
(P < 0.05). Also, the pool of microbial biomass N varied among sampling dates; all forests had the largest microbial N pool in the dry season (P < 0.05; Table 2) reflecting nutrient immobilization during the rainless period. Interestingly, the lowest pool of microbial biomass N varied among forests. Early- and mid-successional forests had the lowest pools of immobilized N at the beginning of the rainy season, whereas late-successional and primary forests showed the lowest values at the height of the rainy season. In addition, the variation of the microbial biomass C:N ratio among sampling dates was highly different among forests according to the successional stage (Table 2). Late-successional and primary forests had the lowest N immobilization per gram of C at the beginning of the rainy season. In contrast, N immobilization per gram of C in soils from early- and
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Table 3 Pools of mineral N and indexes of potential soil N cycling for different seasonally dry tropical forests studied at Sierra de Huatla, Mexico Forest Primary
Early-successional
Mid-successional
Late-successional
2.9 (0.3)b1 1.0 (0.2)a1 3.5 (1.7)b1
4.2 (0.3)a2 1.1 (0.3)a3 6.8 (1.0)a1
4.7 (0.7)a2 0.9 (0.2)a3 8.7 (0.3)a1
4.9 (0.8)ab1 1.1 (0.2)a2 6.7 (1.1)a1
0.6 (0.1)b1 0.2 (0.1)b2 0.2 (0.1)b2
1.3 (0.3)a1 0.5 (0.2)ab12 0.3 (0.1)ab2
1.2 (0.2)a1 0.8 (0.1)a12 0.5 (0.1)a2
0.9 (0.2)ab1 0.6 (0.1)a1 0.3 (0.1)ab2
Potential N mineralization (g m2 per day) Dry season 0.8 (0.5)c2 Rainy season (beginning) 0.3 (0.6)a2 Rainy season (midway) 2.3 (0.8)c1
2.2 (0.6)a2 1.6 (0.6)a2 5.3 (0.6)ab1
2.0 (0.4)a2 1.2 (0.5)a2 8.0 (0.5)a1
0.8 (0.4)b2 1.1 (0.7)a2 4.5 (0.4)b1
Potential nitrification (g m2 per day) Dry season 1.1 (0.2)b2 Rainy season (beginning) 0.2 (0.1)b2 Rainy season (midway) 2.3 (0.7)c1
2.4 (0.6)a2 0.8 (0.2)a3 5.3 (0.6)b1
2.8 (0.5)a2 0.5 (0.2)ab3 8.1 (0.1)a1
1.6 (0.7)ab2 0.3 (0.3)ab3 4.6 (0.5)b1
2
NO3–N (g m ) Dry season Rainy season (beginning) Rainy season (midway) NH4–N (g m2) Dry season Rainy season (beginning) Rainy season (midway)
Data are means (standard error). Different letters (a, b, c) indicate means are significantly different (P < 0.05), when testing for differences among forest within each time period. Different numerals (1, 2, 3) indicate means are significantly different (P < 0.05), when testing for changes through time within a forest.
mid-successional forests was over 50% higher at the beginning of the rainy season (P < 0.01). 3.2. Soil mineral N and potential N-transformation pools The mineral N pools (NO3 and NH4) were the lowest in the mature forests (Table 3). In addition, in successional forests there were significant differences in these pools among sampling dates. In the middle of the rainy season, soil NO3 pools were almost six-fold those determined at the beginning of the season (P < 0.01). Although temporal changes in the NH4 pools were noted in all successional forests, the pattern was not the same as shown by NO3. The NH4 pools were the highest in the dry season, when plant uptake is minimal, and decreased during the rainy season (by 50% to a factor of three; P < 0.05). Potential N mineralization and nitrification differed among forests influenced by the successional stage (Table 3). The potential N transformation was the lowest in late-successional and primary forests, i.e., the oldest forest. In general, relative rankings of the sites for each of the parameters of potential soil N turnover changed little from date to date. However,
these indexes of potential N transformation exhibited a high temporal variability. For example, there was a significant effect of sampling date on potential N mineralization (P < 0.01) and potential nitrification (P < 0.05); both potential N transformations were almost twice higher in the rainy season (at midway through) than in the other sampling dates. This significant increase in potential N transformations is consistent with both the time period increase between the start of the rainy season and the sampling date, and the large amount of rainfall accumulated.
4. Discussion A number of studies have compared the levels of soil and microbial biomass nutrients in a single forest over time or with nearby pasture or other disturbed areas (Singh et al., 1989; Campo et al., 1998; Galicia and Garcı´a-Oliva, 2004). No studies were found comparing the seasonal effects of rainfall on the soil microbial biomass in secondary versus primary forests. When such comparisons were made during the course of this study we found large differences in pools of microbial biomass C and potential N cycling
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between early- and mid-successional forest soils and late-successional and primary forest soils, even though all sites were 2 km away from each other with the same climate and soil conditions. In general, early- and mid-successional forest soils had the greatest pools of microbial biomass C, total and mineral N. For example, pools of total soil N increased from 90 to 150 g m2 in mature forest sites to 180 to 250 g m2 in successional forest sites. We also found great differences in potential soil N transformations between the early- and mid-successional forests and the late-successional and primary forests; the highest and lowest potential transformations were measured in both sets of forest soils, respectively. These results suggest that the recovery of N dynamics processes in the case of seasonally dry tropical forest soils of Morelos, Mexico, occurs during ca. 60 years of secondary succession. This hypothesis needs to consider site-specific differences in N cycling processes. The differences in N cycling among forests appear to reflect the aboveground N flux in litterfall (Table 1) and are consistent with the relative importance of leguminous trees (relative importance values ranged from 56 to 63% and 23 to 34%, in early- and midsuccessional forests and in late-successional and primary forests, respectively; Campo, unpublished data). These results are consistent with those found in tropical humid forests of Puerto Rico by Erickson et al. (2001), where the rates of soil N transformations are related with litter quality (C:N ratio). Leguminous often have larger amounts of litterfall N (see Binkley and Giardina, 1998), and it may directly influence soil N transformations (Scott and Binkley, 1997). Thus, the difference in soil N pools and potential transformations among our sites suggests that this is a major mechanism whereby plant communities influence the recovery of N cycling processes. The microbial biomass C and N pools in the different age forests were affected by the start of the rainy season. Interestingly, the results of this study show a striking contrast in the effect of rainfall seasonality on the primary and late-successional forests in comparison with forests in early- and mid-successional stages of secondary succession. The start of the rainy season leads to a high increase in both the microbial biomass C pool and its ratio C:N in the soils of the early- and midsuccessional forests, where N pools and N cycling are the highest; whereas in late-successional and primary
forests the onset of the rain leads to a decrease in both parameters measured. Studies of soils from other primary seasonally dry tropical forests (Singh et al., 1989; Campo et al., 1998) also have reported a large decrease of the microbial biomass following the start of the rainy season. In addition, although all forests showed the highest pool of microbial biomass N in the dry season, the effect of the rainy season could have strong differences according to the successional stage of forests (Table 3). Differences in response of the soil microbial biomass to the start of the rainy season in the forests under study have important consequences for nutrient cycling in these seasonal ecosystems. Our study on the consequences of aging of the secondary forest following the cessation of agricultural practices which caused soil changes in Morelos, Mexico, allows us to conclude that the nutrient dynamics in those ecosystems depends on the successional stage of the forests. We have shown that soil C and N dynamics are restored after ca. 60 year of secondary succession. Given the potential for tropical forest regeneration after the impact of land use on tropical ecosystems, the topic of the present study warrants subsequent investigations Acknowledgements We thank to A. Elton for help with the site selection, and to E. Solı´s, for valuable help in the laboratory. Special thanks go to personnel from the Centro de Educacio´ n Ambiental e Investigacio´ n Sierra de Huatla of the Universidad Auto´ noma del Estado de Morelos: O. Dorado and A. Mata for their logistical help during this study. This research was supported by the CONACYT under grant N-31954. We thank two anonymous reviewers for helpful suggestions on an earlier version of the paper.
References Anderson, J.M., Ingram, J.S.I., 1993. Tropical Soil Biology and Fertility. A Handbook of Methods. CAB International, Wallingford, 221 pp. Binkley, D., Giardina, C.P., 1998. Why do tree species affect soils? The Warp and the Woof of tree–soil interactions. Biogeochemistry 42, 89–106. Brookes, P.C., Landman, A., Pruden, G., Jenkinson, D.S., 1985. Chloroform fumigation and the release of soil nitrogen: a rapid
V. Saynes et al. / Applied Soil Ecology 29 (2005) 282–289 direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol. Biochem. 17, 837–842. Campo, J., Jaramillo, V.J., Maass, J.M., 1998. Pulses of soil phosphorus availability in a tropical dry forest: effects of seasonality and level of wetting. Oecologia 115, 167–172. Dorado, O., 1997. Sustainable development in the tropical deciduous forest of Mexico: myths and realities. In: Hoagland, A.E., Rossman, A.Y. (Eds.), Global Genetics Resources: Access, Ownership and Intellectual Property Rights. Associations of Systematic Collections, Washington, pp. 263–278. Eaton, W.D., 2001. Microbial and nutrient activity in soils from three different subtropical forest habitats in Belize. Central America before and during the transition from dry to wet season. Appl. Soil Ecol. 16, 219–227. Erickson, H., Keller, M., Davidson, E.A., 2001. Nitrogen oxide fluxes and nitrogen cycling during postagricultural succession and forest fertilization in the humid tropics. Ecosystems 4, 67– 84. Galicia, L., Garcı´a-Oliva, F., 2004. The effects of C, N and P additions on soil microbial activity under two remnant tree species in a tropical seasonal pasture. Appl. Soil Ecol. 26, 31–39. Garcı´a, E., 1988. Modificaciones al Sistema de Clasificacio´ n Clima´ tica de Ko¨ ppen. Universidad Nacional Auto´ noma de Mexico, Mexico, 217 pp. Jenkinson, D.S., 1988. The determination of microbial biomass carbon and nitrogen in soil. In: Wilson, J.R. (Ed.), Advances
289
in Nitrogen Cycling in Agricultural Ecosystems. CAB International, Wallingford, pp. 368–386. Lodge, D.J., Mc Dowell, W.H., Mc Swiney, C.P., 1994. The importance of nutrient pulses in tropical forest. Trends Ecol. E 9, 384– 387. Paul, E.A., Clark, F.E., 1996. Soil Microbiology and Biochemistry. Academic Press, San Diego, 368 pp. Robertson, G.P., Wedin, D., Groffman, P.M., Blair, J.M., Holland, E.A., Nadelhoffer, K.J., Harris, D., 1999. Soil carbon and nitrogen availability. Nitrogen mineralization, nitrification, and soil respiration potential. In: Robertson, G.P., Coleman, D.C., Bledsoe, C.S., Sollins, P. (Eds.), Standard Soil Methods for Long-Term Ecological Research. Oxford University Press, New York, pp. 258–271. Scott, N.A., Binkley, D., 1997. Foliage litter quality and annual net N mineralization: comparison across North American forest sites. Oecologia 111, 151–159. Singh, J.S., Raghubanshi, A.S., Singh, R.S., Srivastava, S.C., 1989. Microbial biomass acts as a source of plant nutrients in dry tropical forest and savanna. Nature 338, 499–500. Trejo, I., Dirzo, R., 2000. Deforestation of seasonally dry tropical forest: a national and local analysis in Mexico. Biol. Conserv. 94, 133–142. Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass. Soil Biol. Biochem. 19, 703–707.
