Analyzing vegetation cover-induced organic matter mineralization dynamics in sandy soils from tropical dry coastal ecosystems

Catena 185 (2020) 104264

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Analyzing vegetation cover-induced organic matter mineralization dynamics in sandy soils from tropical dry coastal ecosystems

T

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Adolfo Campos C.a, , Gabriela Suárez M.b, Javier Labordea a b

Instituto de Ecología, A. C., Apartado Postal 63, CP 91000 Xalapa, Veracruz, Mexico Universidad Veracruzana, Mexico

A R T I C LE I N FO

A B S T R A C T

Keywords: Soil C and N mineralization Tropical semi-deciduous forest Secondary forest Dune scrub Sandy soil properties

To gain knowledge about carbon and nitrogen mineralization potentials and their interaction with sandy soil environment in tropical dry coastal ecosystems, we carried out a short-term laboratory incubation experiment. For this, soil surface (0–10 cm) samples were collected from tropical semi-deciduous forest (TSdF), secondary forest (SecF), coastal dune scrub_crest (DS_C), and coastal dune scrub_slack (DS_S). Soil samples were incubated at 25 °C with constant soil moisture (at field capacity) for 97 days, and over this time 10 and 11 sampling occasions were analyzed to determine carbon (CO2-C) and nitrogen (NH4+ , NO3−) dynamics, respectively. We used a simple exponential model to estimate soil carbon and nitrogen mineralization pools. On average, soil organic carbon mineralization rates ranged between 0.017 and 0.053 mg CO2-C g−1 soil d−1 and varied in the following order: DS_S > SecF > TSdF > DS_C. Average net mineralization rates (mg N kg−1 soil d−1) ranged between 16.9 and 18.8 and varied in the following order: SecF > DS_S > TSdF, whereas in DS_C it was −0.44, indicating N immobilization. Co and No represented, on average, 1.08% and 5% of soil organic carbon and total organic nitrogen, respectively. On average, mineralization constants (k) for Co and No were 0.29 d−1 and 0.23 d−1, respectively, showing that SOM is easily mineralized. The proportion of NO3−/ Nm was very high in SecF (89%) and TSdF (75%), while DS_C showed nitrate immobilization. The increase in NO3−/ Nm ratio in SecF could be associated with legume species that have established in the nature restoration (SecF) on ex-grassland. Across all study sites, linear regression analyses suggested that soil physical and chemical properties may regulate SOM mineralization (p < 0.05).

1. Introduction Soils play a major role in many global biogeochemical cycles, due to their position at the interface between the atmosphere and lithosphere (Rasmussen et al., 2015). For example, soils govern nutrient flux between the lithosphere and vegetation and are also sources and sinks of gases to the atmosphere (Rasmussen et al., 2015; Lal, 2016). Thus, it is clear that vegetation and its associated soils are tightly interlinked and influence each other during successional changes in developing ecosystems (Bauer et al., 2015). A quantitative description of the evolution through time of processes and properties within soils is therefore of great interest (Scharlemann et al., 2014; Lal, 2016). Sandy soils have natural low production potential, due to limiting soil conditions such as low water retention capacity, high water infiltration, low nutrient and carbon storage, and high erosion susceptibility, all of which make at ecosystem naturally fragile (Bruand et al., 2005; Soares et al., 2015). The sandy texture of large-sized, low-specific area grains creates large

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macropores, reducing soil water retention capacity and decreasing the available water content in soil (Bruand et al., 2005). Soil organic matter (SOM) is a particularly important component in terrestrial systems because it provides nutrients to plants when decomposed and increases nutrient holding capacity and water holding capacity (Wood et al., 2016). Removing carbon dioxide (CO2) from atmosphere (via photosynthesis) and storing the carbon (C) in resistant soil organic matter is a global priority for restoring soil fertility and helping to mitigate climate change (Kutsch et al., 2009; Lal, 2016). However, many coastal ecosystems are exposed to intensified human use, resulting in the loss of soil organic matter. Soil organic carbon (SOC) and nitrogen (N) mineralization are fundamental biogeochemical processes that maintain soil fertility and vegetation production (Davidson and Janssens, 2006). A better understanding of the mineralization of SOC and N in soil is necessary in order to improve soil fertility management, which would contribute to food security and climate change mitigation (Davidson and Janssens, 2006;

Corresponding author. E-mail address: [email protected] (A. Campos C.).

https://doi.org/10.1016/j.catena.2019.104264 Received 19 September 2017; Received in revised form 13 September 2019; Accepted 15 September 2019 0341-8162/ © 2019 Elsevier B.V. All rights reserved.

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Fig. 1. Location of the study area showing overview of the sampling plots for each vegetation cover type.

et al., 2009; Sanderman et al., 2014). We need to understand how soil organic matter pools, as a major player in global carbon and nutrient cycles, respond to the mineralization process and associated changes with land cover. Soil organic matter mineralization is vital for predicting how environmental changes may influence the dynamics and availability of C and N in sandy soils. Identifying soil properties that contribute to the stability of soil organic matter constitutes a research priority of regional and global relevance. Therefore, a laboratory incubation experiment was carried out in sandy soils in tropical dry coastal ecosystems. The aim of this experiment was to examine variations in soil C and N mineralization as a function of ecosystem type in sandy soils, to identify links between soil chemical and physical properties and SOM mineralization throughout the ecosystem types studied, and to address relationships between soil properties and SOM mineralization on a regional scale. We hypothesized that, across tropical dry coastal ecosystems, processes of C and N mineralization would be explained by ecosystem type and soil physical and chemical properties, and that the forest restoration process from ex-grassland would stimulate soil C and N mineralization due to increases in soil nutrient availability.

Lal, 2003). In soil, organic matter is present as a continuum of biomaterials that are constantly mineralized by soil microbes to smaller molecular size (Kleber et al., 2015; Lehmann and Kleber, 2015). It has been shown that the stability and mineralization of soil organic matter is linked to the formation of organo-mineral complexes through chemical or physicochemical interactions with minerals and metal ions, as well as to physical protection within soil aggregates (Hassink, 1997; Baldock and Skjemstad, 2000; Kögel-Knabner et al., 2008). All this highlights the soil's capacity for organic carbon storage, depending mainly on the soil mineralogy, composition of the organic matter input, and certain environmental factors (Kleber et al., 2015; Kögel-Knabner, 2017; Singh et al., 2018). For example, organic matter composed of plant litter is considered to have faster mineralization rates compared to organic matter bound to the soil mineral fraction and polyvalent cations–which, in turn, are considered more resistant to microbial mineralization (Cotrufo et al., 2013; Ahrens et al., 2015). Soil organic carbon and total nitrogen are two important components with key roles in mitigating global warming, increasing below and aboveground biomass production, and decreasing ecosystem disturbance in order to preserve biodiversity (Davidson and Janssens, 2006; Lal, 2003). Carbon and nitrogen mineralization are closely coupled processes during the decay of plant residues in or on soil, although Müller et al. (2016) suggest that they are decoupled from the mineral-associated fractions of the soil where the interactions of both C- and N-containing components strongly modulate mineralization dynamics (from Kögel-Knabner, 2017). Soil N mineralization is the process by which soil organic N is mineralized into inorganic forms (NH4++NO3−); simultaneously, mineralized inorganic N can be immobilized into organic forms (Neeteson and Hassink, 1993). Estimating the C and N pool mineralized from soil organic matter provides a crucial component in modeling soil C and N dynamics and ecosystem responses to changing environmental factors. SOM mineralization dynamics can be influenced by many factors, such as the quality of organic inputs, nutrient availability, and climate-related factors (Kutsch et al., 2009; Rabbi et al., 2015). The effects of such factors on SOM mineralization have been investigated through shortterm laboratory incubation studies under controlled conditions (Ahn

2. Materials and methods 2.1. Study area The soil samples used in the laboratory incubation experiment were collected from tropical semi-deciduous forest (TSdF), secondary forest (SecF) that was 17 years old (ex-grassland used for grazing purposes), coastal dune scrub_crest (DS_C), and coastal dune scrub_slack (DS_S), located (with central coordinates 19° 36́ N, 96° 23́ W) on the coastal plain of the Gulf of Mexico (Fig. 1). The soil is derived from sand dunes, with very high sand and very low clay content, very weak soil structure, and rolling landscape (e.g. DS). Climatic conditions during the observation period appear in Fig. 2. The total mean annual rainfall was 1258.5 mm. Most of the rainfall (approx. 83%) occurred in four months, from June to September. The mean annual temperature was 24.8 °C, 2

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30

700

28

600

26 24 22

400

20 300

Mean temperatures 2012 2013 2014

200

18 16

Temperature (°C)

Rainfall (mm)

500

14 100

12 10

0 0

2

4

6

8

10

12

Month Fig. 2. Mean monthly rainfall distribution (bars). The red curve represented the mean value of monthly temperatures for 2012, 2013, and 2014. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

determined for all soil samples using acid neutralization method (van Reeuwijk, 2006). The aggregate size distribution was determined by dry sieving through a rotary sieve (Chepil, 1962). The following aggregate size classes were separated: > 2 mm, 0.25–2 mm (macroaggregates), < 0.25–0.15 mm, < 0.15–0.05 mm, and < 0.05 mm (microaggregates). The Ks of the undisturbed soil cores was determined using the constant head method (Klute and Dirksen, 1986). Field capacity (θFC) and the permanent wilting point (θWP) of the soil samples broken by hand were determined at 10 kPa and 1500 kPa pressures, respectively, using membrane plates and pressure chambers (Soil Moisture Equipment Corp., Santa Barbara, CA, USA) (Dane and Hopmans, 2002). At each pressure level, the sample was weighed before each increase in pressure. At the end, the gravimetric water content of the soil was determined by oven drying at 105 °C for 48 h. Soil available water (θAW) was calculated as the difference between the water content values at field capacity (θFC) and the permanent wilting point (θWP).

with the hottest month being June (27.2 °C) and the coldest January (20.6 °C). At DS_C and DS_S sites there is a formation of patches of exposed, loose sand (non-vegetated sand areas). The absence or scarcity of vegetative cover exposes the sandy material to erosive agents, especially to the wind, which favors the movement of soil particles (MorenoCasasola and Travieso-Bello, 2006). 2.2. Soil sampling and laboratory analysis Soil samples from 0 to 10 cm depth were taken from three points at each vegetation cover, as defined as follows. Each experimental area was divided into three portions on its shortest side. At the center of each portion, one transect perpendicular to the baseline was established for soil sampling. At each transect, five subsamples were taken at regular intervals and were then combined into a large composite sample and placed in a plastic bag. Also, at each transect, two undisturbed soil cores were collected at regular intervals in PVC cylinders (diameter 7 cm; length 10 cm) to measure saturated hydraulic conductivity (Ks); three undisturbed soil cores were collected using PVC cylinders (diameter 4.7 cm; length 3.0 cm) to determine soil bulk density. In the laboratory, soil composite samples were air-dried and a portion was ground to pass through a 2 mm sieve for physical and chemical analyses. The remainder was broken by hand for the incubation experiment. Soil samples were analyzed for texture, organic carbon (C), total nitrogen (N), pH, electrical conductivity (EC), exchangeable cations (Ca2+, Mg2+, K+, Na+), cation exchange capacity, and available phosphorus. The sand was fractionated by dry sieving; silt and clay fractions were determined using the pipette method (Gee and Bauder, 1986). Soil sample pH was determined using an electrode pH meter in a 1:2 soil-to-water ratio (Thomas, 1996). EC was measured in saturated paste extract (Rhoades, 1996). Soil organic carbon was determined by the Walkley and Black dichromate oxidation method (Nelson and Sommers, 1996). Soil total nitrogen was determined by the Kjeldahl method (Bremner, 1996). Exchangeable cations (Ca2+, Mg2+, K+, Na+) were extracted with NH4OAc buffered at pH 7 (Thomas, 1982) and analyzed using atomic absorption spectrometry (Ca2+, Mg2+) and flame photometry (K+, Na+). Available phosphorus was measured using the Olsen method (van Reeuwijk, 2006). Equivalent calcium carbonate was

2.3. Laboratory incubation experiment We used a short-term aerobic incubation procedure to estimate the potential of sandy soils to mineralize soil organic matter. An aerobic incubation experiment of 97 days was carried out from May 2013 to September 2013. Twenty grams (oven-dry weight equivalent) of soil samples broken by hand were transferred into a 100 mL plastic bottle and wetted to field capacity (corresponding to soil water potential of 10 kPa); these were placed in a 1 L polypropylene jar with a 100 mL plastic screw-capped vial containing 20 mL 0.25 M NaOH to trap respired CO2. Distilled water was added to the jar to maintain a moisturesaturated atmosphere and minimize soil water loss during incubation. Three blank replicates (measuring-jars containing no soil, but water and the NaOH vial) were subjected to the same procedure. After removing the vial from the jar, BaCl2 was added to NaOH to precipitate any carbonate, plus a few drops of phenolphthalein. Thus, CO2 captured in NaOH was titrated with standardized HCl until the solution turned pink. Soil samples were incubated in triplicate at 25 °C in a ventilated incubator. Soil moisture was kept constant throughout the incubation period through weekly weighing and readjusting with distilled water as 3

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3. Results and discussion

needed. Respired CO2 trapped in alkali solutions was measured on days 1, 2, 3, 7, 10, 27, 35, 45, 66, and 97. Inorganic nitrogen was determined by extraction of each sample at 11 sampling occasions (including day 0). The following scenario was considered: each sample was located in its proper air-tight measuring-jar, and CO2-C was measured until the sample had to be removed from the system for further inorganic N extraction (Thuriès et al., 2000).

3.1. Soil classification According to morphology and particle size distribution through the profile, soils on the research sites can be divided into two groups. One is related to sand dunes, including mobile and semi-fixed dunes. The other is related to sandy soils derived from fixed dunes or stabilized sites, which show a more or less advanced stages of soil development. For the first group, the typical pedon for the DS_C site has an A/C horizon to 10 cm, C1 to 30 cm, C2 to 90 cm, and C3 to > 140 cm. In the DS-S site, the typical pedon has an A1 horizon to 5 cm, A/C to 37 cm, C to 83 cm, and IIBw to > 120 cm. In these pedons, all soil horizons have a sandy texture; the sand and clay content was > 90% and < 3.2%, except for the IIBw horizon (with loamy sand texture) which was 81% and 10%, respectively. All soil horizons were dominantly single grained (sandy) except the IIBw horizon, which contained a very weak subangular blocky structure. For the second group, the typical pedon for the TSdF site has an A11 horizon to 14 cm, A12 to 72 cm, A3k to 116 cm, and Bw/C to > 140 cm. In the SecF site, the typical pedon has an A11 horizon to 14 cm, A12 to 39 cm, A3 to 58 cm, Bw to 85 cm, and IIBwk to > 120 cm. In these pedons, most genetic horizons have a loamy sand texture, where the sand and clay content was > 80% and < 10.2%, respectively. Only the Bw (63.3% sand, 16.7% clay) and Bwk (56.6% sand, 24.3% clay) horizons have a sandy loam and sandy clay loam texture, respectively. All A horizons usually have a weak fine granular structure. Subsoil layers (A3, Bw/C, Bw horizons) are more compacted than topsoil and have a weak subangular blocky structure. The soils were classified according to WRB (IUSS Working Group WRB, 2015) as Calcaric Arenosols (Aeolic, Colluvic) for sites DS_C and DS_S and Calcaric Cambisols (Arenic) for sites TSdF and SecF.

2.4. Measurements of CO2-C and inorganic N During the 97-day incubation period, CO2-C and inorganic N (NH4++NO3−) production were taken as parameters for microbial activity. They were measured regularly, and at the end of the experiment C and net N mineralization were determined. The amount of CO2-C was calculated from the following formula (Anderson, 1982):

CO2 − C (mg ) = (VB − VS ) ∗ NE where VB is the volume (mL) of acid used to titrate the blank, VS the volume (mL) of acid used to titrate the treatment, N the normality of titrating acid and E = 6 (equivalent weight of C). Data are expressed as milligrams of CO2-C per gram per day. To determine inorganic N content, soil samples were extracted for 1 h with 2 M KCl (1:10 w/v soil:solution ratio) in a reciprocating shaker at 180 reciprocations per min. After shaking, samples were centrifuged (4 min; 3500 rev min−1) and the supernatant was filtered through Ahlstrom 94 paper. The extract was treated with 0.2 g MgO to determine only NH4+, and NO3− was released in a second distillation after adding 0.2 g Devarda'ś alloy (Mulvaney, 1996). Soil net N mineralization rates were calculated from the differences in inorganic N (NH4++NO3−) concentrations between the initial and post incubation soil samples. All results are expressed on an oven-dried weight basis.

3.2. Basic soil properties (0–10 cm depth) The basic chemical and physical properties of soil samples (0–10 cm depth) are summed up in Table 1. The soil samples were all very sandy, ranging from 84% to 94.6%. Silt-sized particles ranged from 4.1% to 9.7%, while clay-sized particles ranged from 1.1% to 6.2%. Clay and silt particles were a little higher under TSdF and SecF than under DS_S and DS_C. The soil reaction across the study area ranged from near neutral (SecF), slightly alkaline (TSdF, DS_S) to moderately alkaline (DS_C). The high pH of surface soils in the study area could be attributed to the parent material (dunes) and weathering processes (Dubroeucq et al., 1992). For example, the CaCO3 concentrations in coastal dune sites were > 8.8%, while in SecF and TSdF sites they were 4.37% and 2.13%, respectively. The organic carbon content ranged from 0.69% to 3.2% and increased in the following sequence: DS_C < TSdF < SecF < DS_S, while total nitrogen content ranged from 0.07% to 0.3% and increased in the following order: DS_C < TSdF < DS_S < SecF. The phosphorus (P) content was generally low, ranging from 1.2 mg kg−1 to 16.1 mg kg−1 and increasing in the following order: DS_C < SecF < TSdF < DS_S. Phosphorus availability in soils is affected by several factors such as the amount of free CaCO3 and Ca2+ ion activity (Brady and Weil, 2002). The interaction of soluble phosphate and soil Ca2+ ions occurs and produces dicalcium phosphate, which over time transforms to tricalcium phosphate as well as phosphorus adsorbed on a calcite surface, leading to a decrease in soil phosphorus availability (Brady and Weil, 2002). The concentrations of exchangeable Ca and Na were particularly high in all the studied ecosystems except for DS_C. On the other hand, concentrations of exchangeable Mg and K were greater in TSdF, SecF, and DS_S than in DS_C. The cation exchangeable capacity (CEC) differed little in TSdF, SecF, and DS_S, ranging from 16.2 cmol kg−1 to 17.8 cmol kg−1, whereas CEC was lower in DS_C. In short, sandy soils in the study area have low nutrient retention capacity due to low clay and organic matter contents. The higher Ks values recorded at DS_S and DS_C sites may be due to the higher sand and lower clay

2.5. Experimental design and data analyses The laboratory incubation experiment was carried out in a completely randomized design with three replicates. The effects of incubation dates and vegetation cover, as well as their interactive effects on soil organic matter mineralization, were determined by repeated measures following the general linear model with incubation dates as a repeated measure and replication as a random effect. Linear regression analyses were used to determine the association between measured soil properties and soil organic matter mineralization. All statistical analysis was done using SigmaPlot 13 (2013). Differences were considered statistically significant at p ≤ 0.05. Using non-linear regression analysis (SigmaPlot 13, 2013), cumulative data on C and N mineralization for soil samples were adjusted to the simple exponential model (Stanford and Smith, 1972; Murwira et al., 1990) as follows:

Cm = CO (1 − e−kt ) where Cm is the amount of mineralized C (mg CO2-C g−1) during the incubation experiment, CO (mg CO2-C g−1) the potentially mineralized C pool, k (day−1) the C mineralization rate constant, and t the incubation time (day). The potentially mineralized N pool and mineralization rate constant were also obtained using the simple exponential model, according to Campbell et al. (1984):

Nm = NO (1 − e−kt ) where Nm is the amount of mineralized N (mg kg−1) during the incubation experiment, NO (mg N kg−1) the potentially mineralized N pool, k (day−1) the N mineralization rate constant, and t the incubation time (day). 4

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Table 1 Soil chemical and physical properties for different ecosystem types. Site abbreviations are as follows: TSdF = tropical semi-deciduous forest; SecF = secondary forest; DS_S = coastal dune scrub_slack; DS_C = coastal dune scrub_crest. Data (n = 3) are expressed as mean ± standard error. Soil parameters

Study sites TSdF

SecF

DS_S

DS_C

pH (H2O) C, % N, % C/N Ca, cmol kg−1 Mg, cmol kg−1 Na, cmol kg−1 K, cmol kg−1 P, mg kg−1 CEC, cmol kg−1 CaCO3, % Sand, % Silt, % Clay, % EC (dS m−1) Ks (cm h−1) θFC (%) θWP (%) θAW (g g−1) BD (g cm−3)

7.1 ± 0.16 2.4 ± 0.40 0.26 ± 0.03 8.9 ± 0.79 13.6 ± 0.91 2.3 ± 0.42 0.78 ± 0.08 0.35 ± 0.05 7.0 ± 1.72 16.2 ± 1.42 2.13 ± 0.29 84.0 ± 0.79 9.7 ± 0.24 6.2 ± 0.96 0.60 ± 0.30 37.3 ± 5.03 15.8 ± 0.02 9.18 ± 0.47 0.06 ± 0.004 1.06 ± 0.02

6.8 ± 0.12 2.8 ± 0.30 0.3 ± 0.006 9.3 ± 0.90 13.1 ± 1.6 1.3 ± 0.44 0.94 ± 0.07 0.49 ± 0.05 6.3 ± 2.06 16.2 ± 2.26 4.37 ± 0.82 87.4 ± 1.91 8.7 ± 2.48 3.8 ± 0.72 1.1 ± 0.02 32.7 ± 6.02 15.9 ± 1.90 7.8 ± 1.27 0.08 ± 0.008 1.1 ± 0.02

7.2 ± 0.26 3.2 ± 2.38 0.29 ± 0.20 9.9 ± 1.01 12.2 ± 5.17 1.5 ± 0.95 1.0 ± 0.59 0.50 ± 0.32 16.1 ± 14.9 17.8 ± 10.2 9.0 ± 0.18 93.1 ± 1.01 4.9 ± 0.42 1.8 ± 0.61 1.0 ± 0.44 50.9 ± 5.39 20.8 ± 14.5 12.7 ± 9.23 0.08 ± 0.05 0.83 ± 0.26

7.8 ± 0.11 0.69 ± 0.27 0.07 ± 0.01 8.9 ± 1.49 6.4 ± 0.96 0.36 ± 0.11 0.35 ± 0.09 0.10 ± 0.05 1.2 ± 0.27 2.7 ± 1.03 8.84 ± 0.1 94.6 ± 0.30 4.1 ± 0.37 1.1 ± 0.23 0.59 ± 0.24 59.4 ± 2.70 6.8 ± 0.49 3.1 ± 1.05 0.03 ± 0.008 1.2 ± 0.01

Macroaggregates (%) > 2 mm 0.25–2 mm

7.58 ± 3.3 35.6 ± 4.2

5.15 ± 0.83 18.7 ± 1.8

0.0 0.0

0.0 0.0

Microaggregates (%) < 0.25–0.15 mm < 0.15–0.05 mm < 0.05 mm

56.8 ± 2.9 0.0 0.0

76.1 ± 2.6 0.0 0.0

83.1 ± 2.9 16.4 ± 2.8 0.37 ± 0.09

83.5 ± 2.4 16.1 ± 2.3 0.34 ± 0.09

nutrients, etc., resulting in faster organic carbon mineralization in comparison with the other sites (Fig. 3b). However, the quasi absence of mineralization flux at DS_C may be due to an inherent reduced accumulation of soil organic carbon (Fig. 3b and Table 1). The sequestration of stable soil organic carbon is attributed to several mechanisms, including physical protection of soil aggregates and the formation of organo-mineral interactions with fine (i.e. clay and silt) soil particles (Tisdall and Oades, 1982; Kleber et al., 2015; Singh et al., 2018). In sandy soils such as those of the study site, the formation of aggregates and fine fraction complexes are markedly restricted, due to the low amount of clay and silt, especially at DS_S and DS_C sites. As a consequence, the high organic carbon mineralization observed at DS_S is attributable to the fact that organic material around sand particles has little or no physical protection, making it the most bioavailable organic matter fraction (Hassink, 1995; Singh et al., 2018). In sandy soils, organic carbon is more easily accessible to soil microbes than in clay soils (Singh et al., 2018). This suggests that the inputs consisting primordially of plant residues in low lying hollows (i.e. DS_S sites) between dune ridges are very early mineralized, increasing nutrient availability and creating more fertile conditions than at DS_C sites, thus regulating vegetation growth functions. This provides clear evidence that DS_S sites have great potential to sequester organic carbon into the soil via litter input. However, due to null physical protection, their vulnerability to microbial attack increases, leading to an accelerated loss of soil organic carbon. In comparison to that of DS_S sites, the soil organic carbon of TSdF and SecF exhibited more efficient mineralization, probably due to the greater proportion of fine (clay and silt) particles and macroaggregates found there, as well as to a higher level of organo-mineral interactions (Hassink, 1992; Yu et al., 2017; Ellerbrock and Gerke, 2018). This is manifested in rapidly declining carbon mineralization rates (Fig. 3a). Thus, it appears that fine particles (clay and silt), the amount of macroaggregates and microaggregates, as well as available organic carbon, controlled the mineralization pattern, especially at DS_C, where organic

contents than at TSdF and SecF sites. Results show almost no differences in soil available water (θAW) data for TSdF, SecF, and DS_S sites, while the lowest θAW values were observed at the DS_C site. High bulk density is primarily due to the very high sand content, although the lowest average value observed at the DS_S site may be due to higher organic carbon content than at other sites. The EC means ranged from 0.59 to 1.1 dS m−1 across sites, increasing in the order DS_C < TSdF < DS_S < SecF. The distribution of aggregate size classes showed that microaggregates (mainly large ones) dominated in all sites’ soils, but important portions of macroaggregates (mainly small ones) were present only in forest soils, especially in the TSdF site. In contrast, the aggregate fractions obtained in coastal dune sites consisted only of microaggregates, mainly large ones, with relatively low amounts of small microaggregates.

3.3. The SOC mineralization process The organic carbon mineralization rate (Fig. 3a) ranged between −0.002 (min.) and 0.22 (max.) mg CO2-C g−1 d-1. DS_S and DS_C always featured the highest and lowest carbon mineralization rates, respectively (Fig. 3a). In our experiment, organic carbon experienced a strong initial mineralization at the beginning of the incubation period, followed by a strong decline in the mineralization rate. The cumulative carbon mineralization on day 97 was higher in DS_S (0.53 ± 0.08 mg CO2-C g−1), followed by SecF (0.37 ± 0.03) and TSdF (0.33 ± 0.01), while the DS_C (0.17 ± 0.01) showed lower values (Fig. 3b). The variance in carbon mineralization rates was primarily explained by the time, explaining 55.1% of the variance (Table 2). Despite having a much weaker effect than the previous factor, the contribution of the site × time interaction was significant and explained 12.2% of the variation throughout the incubation period. The strong mineralization flux observed at DS_S may be associated with geomorphic aspects of those sites (due to dune dynamics), which produce a favorable soil environment such as local concentration of litter input, soil moisture, 5

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Fig. 3. Soil organic carbon mineralization rates (a) and cumulative carbon (b) respired as CO2-C (mean ± standard error) from TSdF (tropical semi-deciduous forest), SecF (secondary forest), DS_C (coastal dune scrub_crest), and DS_S (coastal dune scrub_slack) soil samples at 30 °C during the 97-day incubation period (n = 3).

organic matter.

Table 2 Repeated ANOVA analyses to evaluate the two primary factors (site and time of incubation) that influence carbon, nitrogen, ammonium, and nitrate mineralization rates. Source of variation

df

%SS

F

P-value

C mineralization rates (mg g day ) Site 3 0.0197 Time 9 0.0827 Site × Time 27 0.0183 Residuals 54 0.0139

13.1 55.1 12.2 9.2

4.044 61.738 2.634

0.069 < 0.001 0.001

Net N mineralization rates (mg kg−1 day−1) Site 3 7440.9 Time 9 11681.9 Site × Time 27 5929.2 Residuals 54 7017.4

18.9 29.6 15.0 17.8

4.044 9.820 1.690

0.069 < 0.001 0.051

NetNH4+mineralization rates (mg kg−1 day−1) Site 3 555.0 Time 9 1658.8 Site × Time 27 787.8 Residuals 54 1330.4

10.6 31.8 15.1 25.5

10.999 5.868 1.184

0.007 < 0.001 0.292

NetNO3−mineralization rates (mg kg−1 day−1) Site 3 5967.1 Time 9 4783.8 Site × Time 27 4941.9 Residuals 54 3735.3

25.0 20.0 20.7 15.6

3.834 10.908 2.646

0.076 < 0.001 0.001

−1

SS

3.4. Soil N mineralization process There was a sudden and marked transient increase in the organic nitrogen mineralization rate, mainly at TSdF, SecF, and DS_S sites during the first 10 days (Fig. 4a). It decreased over the subsequent and then remained constant for the last 30 days of incubation (Fig. 4a). The cumulative N mineralization on the 97th day of incubation was higher at SecF (188.2 ± 18.60), followed by DS_S (172.30 ± 51.16), TSdF (169.2 ± 8.58), and DS_C (−4.45 ± 21.55). Organic nitrogen is assumed to accumulate in aggregates during the aggregation process of soil particles (Gunina et al., 2015; Wei et al., 2017). Specifically, the proportion of macroaggregates was higher in the TSdF and SecF sites (Table 1), which indicate that these soils were more aggregated compared to those of others sites. N accumulation at SecF, DS_S, and TSdF sites increased rapidly until the 10th day, slowing during subsequent incubation. In contrast, at DS_C sites it remained low, with negative values throughout incubation (Fig. 4b). More specifically, the highest cumulative NH4+ mineralization at day 97 corresponded to DS_S, and the lowest to DS_C, followed by SecF, while TSdF showed intermediate values (Fig. 4d). In the case of cumulative NO3− mineralization, the greatest production was measured at SecF, followed by TSdF and DS_S, while DS_C had lower values (Fig. 4f). Our data showed (Table 2) that variance in the nitrogen mineralization rate was explained by incubation time (29%). When considering the NH4+mineralization rate, variance was explained by time and site (31.8% and 10.6%, respectively), whereas variance in the NO3− mineralization rate was explained equally well by incubation time and its interaction (20.0% and 20.7%, respectively). Generally, more nitrogen was mineralized as NO3− than as NH4+ and thus, nitrification was dominant in these soils, especially at sites with a high N mineralization rate (Table 2). The average ratio of nitrification rate to N mineralization rate was greatest at SecF (89.7%), followed by TSdF (75.8%) and DS_S (59.5%). The negative values of NO3− mineralization rates obtained for DS_C sites revealed that N demands for soil microbial system were insufficient (Schmidt et al., 2011; Schimel and Bennett, 2004; Tian et al., 2017). Research on poor ecosystems where inorganic N does not accumulate over the study period has indicated that N soil availability remains limited (Yevdokimov and

−1

carbon is limited. Then, in SecF and TSdF, the fine fraction and proportion of macroaggregates and microaggregates can limit the bioavailability of soil organic matter due to the interaction between organic molecules, soil clay, and silt particles, as well as organic matter occluded within aggregates, leading to a greater capacity to stabilize soil organic carbon (Balesdent et al., 1998; Elliott, 1986; Marschner and Kalbitz, 2003; Feng et al., 2014; Singh et al., 2018). However, due to still weak physical protection, soil organic matter at these sites (SecF and TSdF) could be extremely vulnerable to vegetation cover perturbation by anthropogenic impacts and global warming, phenomena which in turn affect important biogeochemical variables such as soil carbon and nitrogen dynamics. Our study reveals that DS_S sites store an important fraction of the regionaĺs carbon in soil surface labile

6

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Fig. 4. Net N mineralization rate (a, c, e) and cumulative net N mineralization (b, d, f) from TSdF, SecF, DS_C, and DS_C soil samples at 30 °C during the 97-day incubation period (n = 3).

rates, suggesting that tree species composition might drive N transformation in the ecosystems studied. Singh et al. (2000) reported that tree species composition was an important component influencing N dynamic in various vegetation types.

Blagodatsky, 1994; Isobe et al., 2015). Thus, we can affirm that in the ecosystems studied, there are sites (e.g. SecF, TSdF and DS_S) where N mineralization dominates, maintaining an active cycle of soil N; but there are others (e.g. DS_C) where N immobilization dominates, resulting in limited mineral N for plant growth functions. The microorganisms in the DS_C site are often organic matter limited. The deficiency of energy can strongly affect the balance between the availability of carbon and nitrogen in the soil, as well as the demand of nitrogen and microbial carbon (Tian et al., 2017), which could explain the behavior of the soil nitrogen mineralization observed in the DS_C site. In our analysis, site types affected NH4+ and NO3− mineralization

3.5. Carbon and nitrogen mineralization modeling Parameters calculated according to the simple exponential model are shown in Table 3. In all cases, the model was highly significant (p < 0.006). As can be seen, the size of potentially mineralized C (Co) among sites varied slightly, ranging from 0.15 to 0.48 mg CO2-C g−1, 7

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Table 3 Parameters obtained by fitting the simple exponential model to measured data from the mineralization experiment. Sites

C mineralization Co

TSdF SecF DS_C DS_S

0.29 0.33 0.15 0.48

N mineralization k

± ± ± ±

0.02 0.04 0.02 0.12

0.33 0.28 0.21 0.34

R ± ± ± ±

0.06 0.02 0.03 0.06

2

0.82 0.90 0.84 0.86

No

k

R2

154.7 ± 0.66 173.4 ± 23.7 np 155.7 ± 121.8

0.22 ± 0.02 0.20 ± 0.04 np 0.14 ± 0.05

0.92 0.93 np 0.89

np: indicate that the model did not fit the data.

soil available water, which, in turn, could be linked to soil environmental conditions (i.e. mineral particle-size proportion and SOM content) across sites. For example, DS_C soils with higher levels of sand and an inherently lower accumulation of SOM have lower mineralized C and N values. In addition, landscape variables, such as the presence of hollows in DS_S soils, could explain variation in potentially mineralized C and N values, because hollows accumulate important quantities of organic material as major pathways for carbon sequestration. Soil available water constitutes the main source of water consumed by vegetation and makes the organic substrate accessible to soil microorganisms (Orchard and Cook, 1983; Hosseini et al., 2016). We observed that potentially mineralized C and N were associated with a negative linear correlation to soil bulk density (Fig. 5c and d). Moreover, potentially mineralized N showed a negative correlation with soil hydraulic conductivity (Ks) (Fig. 5e). This pattern may be linked to the fact that denser soils have a smaller surface area, causing a lower capacity to retain organic carbon and moisture (Lobsey and Viscarra Rossel, 2016). As a result, soil physical environment such as soil bulk density and hydraulic conductivity could control biological processes (e.g. SOM mineralization) by regulating gas diffusion rates and water flow within the soil. Specifically, DS_C soils displayed greater hydraulic conductivity than those of other sites, a phenomenon that could derive from the soil's physical environment, including vegetation composition. In particular, sandy soils (i.e. DS_C) have lower water retention capacity, because most pores are large and drain rapidly (Zotarelli et al., 2007). Moreover, at DS sites, the vegetation is discontinuous, consisting of small patches of shrubs separated by areas of bare soil. Linear regression analyses revealed strong associations between soil chemical properties and SOM mineralization (p < 0.05). In line with this, potentially mineralized C was positively related to soil organic nitrogen, whereas potentially mineralized N showed a significant positive correlation with soil organic carbon (Fig. 6a and b). In sandy soils, there is limited protection of organic matter by the mineral matrix. We found significant positive correlations between potentially mineralized C and N with cation exchange capacity (Fig. 6c and d). It is well established that soil cation exchange capacity is the capacity of soil to adsorb and exchange cations (Tan, 2011). In our study, these relationships (Fig. 6c and d) could explain the increase in microbial activity when nutrient concentrations and C availability are increased. Certainly, sandy soils have a very limited cation exchange capacity (e.g. DS_C soils), as they possess little or no electrical charge (Zotarelli et al., 2007; Tan, 2011). In contrast, organic colloidal materials have a much greater CEC per unit weight than mineral colloidal materials (Tan, 2011), leading to an increase in soil nutrient and water retention. This was particularly clear at study sites where SOM (i.e. inputs of plant carbon to soil) could potentially influence soil response to C and N mineralization processes by modifying soil properties. Evidently, SOM has a large effect on CEC due to a number of complex interactions and feedbacks involving soil texture, clay-mineral proportion, and soil water, as well as to the quantity and quality of litter inputs (Murphy, 2015; Kallenbach et al., 2016). In our study, the variation pattern in electrical conductivity

and decreasing in the order DS_S > SecT > TSdF > DS_C. However, the effect of site on Co was not significant (p = 0.05). Additionally, the Co value, expressed as a percentage of SOC, varied very little among the sites. During the 97-day incubation period, between 0.83% and 1.26% of soil organic carbon was released as CO2, with a mean value of 1.08%. Thus, Co/SOC demonstrates that SOC mineralization responds to organic substrate availability due to weak physical protection of SOM within the sandy soil matrix. The mineralization constant (k) of Co ranged from 0.21 to 0.34 d−1 and decreased in the order DS_S > TSdF > SecT > DS_C. The k constant reflects mineralization rates of the labile SOC fraction (Reichstein et al., 2000; Ribeiro et al., 2010; Ci et al., 2015). Thus, in our study, high k values may reflect weak physical protection of organic matter in sandy soils. Furthermore, the narrow range of k values among the sites studied suggests that mineralized organic matter could be of same degree of availability for soil microbial biomass. Regarding accumulated N at the DS_C site, it was not simulated using the simple exponential model because it remained nearly stable over the entire incubation period (Fig. 4b and Table 3). At the other sites, in contrast, No values ranged from 154.7 to 173.4 mg N kg−1 and decreased in the order SecT > DS_S > TSdF. However, the effect of site on No was not significant (p = 0.192). All No values using the simple exponential model are within the range (66–185; 71–250 mg N kg−1) reported by Campbell et al. (1984) and Curtin and Wen (1999), respectively. As shown in Table 3, k values were high and indicated that organic N is easily mineralized and readily used by microorganisms, due presumably to the low capacity of sandy soils to protect organic matter. In our experiment, No represented an average of 5% of total organic N. The ratio of potentially mineralized N (No) to total N represents the active N fraction in SOM. In this context, Weier and MacRae (1993) reported No/ N ratios of between 0.8 and 5.3% for cultivated soil. However, other studies have reportedNo/ N ratios ranging from 5 to 18% at different soil surface layers (e.g. Campbell and Souster, 1982; Cabrera and Kissel, 1988). In this study, the percentage of Cm/ Nm ratios were 1.94 in TSdF, 2.0 in SecF, 6.4 in DS_C and 4.6 in DS_S. These variations indicate that TSdF and SecF were more favorable for the accumulation of C stock than N pool, while DS_C and DS_S were sensitive to N loss or immobilization. In our study, net nitrification did occur, and the proportion of NO3−/ Nm was very high: 89% in SecF, 75% in TSdF, and 62% in DS_S, while DS_C exhibited nitrate immobilization due to substrate limitation. Our findings clearly indicate that ammonium was readily converted to nitrate, especially in SecF. The rise of NO3−/ Nm ratio at the SecF site could be associated with legume (Nfixing) species that grow at nature restoration site and on ex-grassland. N-fixing tree species are capable of increasing N input to soil and litterfall, thus influencing soil N mineralization (Hoogmoed et al., 2014). 3.6. The link between SOM mineralization and soil properties Linear regression analyses showed that soil physical and chemical properties could regulate SOM mineralization (p < 0.05). For example, we found that potentially mineralized C (Fig. 5a) and N (Fig. 5b) values increased when the soil available water content rose, so the trend observed suggests that each ecosystem studied responded differently to 8

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Fig. 5. Impacts of soil physical properties on potentially mineralized C and N in four different ecosystems. All regression lines indicate a significant relationship p ≤ 0.05. Triangle = TSdF, circle = SecF, square = DS_C, diamond = DS_S.

solution (Hillel, 2000). The soil samples studied have EC < 2.0 dS m−1, suggesting that soils of 0–10 cm depth are characterized by low concentrations of salts in the soil solution. Thus, the linearity of the data (Fig. 6e and f) shows the importance of CE’s influence on

throughout the area was positively related to potentially mineralized C and N during the incubation experiment (Fig. 6e and f). It is generally assumed that EC provides a quick estimate of the concentration of electrically-charged water soluble salts able to enter and persist in a soil 9

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Fig. 6. Impacts of soil chemical properties on potentially mineralized C and N in four different ecosystems. All regression lines indicate a significant relationship p ≤ 0.05. Triangle = TSdF, circle = SecF, square = DS_C, diamond = DS_S.

soil respiration was not significantly correlated to EC but that as EC increased, the metabolic quotient (respiration per unit biomass) also went up. We found a negative correlation between the N mineralization rate

potentially mineralized C and N, an influence that was exerted during the SOM mineralization process in the ecosystems studied. Previous research highlighted the importance of EC on prediction of SOM mineralization rates. For example, Rietz and Haynes (2003) reported that 10

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Fig. 7. Relationships between N mineralization rate constants and C:N ratio (a), and between potentially mineralized N and pH (b) for all vegetation cover types. Regression lines indicate a significant relationship p ≤ 0.05. Triangle = TSdF, circle = SecF, square = DS_C, diamond = DS_S.

the presence of macroaggregates, clay content, and Ca2+ ion activity (from CaCO3), all of which are important elements in soil organic carbon stabilization. Generally, more nitrogen was mineralized as NO3− than as NH4+, and for this reason, nitrification was dominant in the soils studied. In particular, the higher NO3−/ Nm ratio in secondary forest (SecF), as compared to other sites, could be due to the establishment of legume (N-fixation) species in the nature restoration process that can occur in ex-grassland. We recognize that the values of NO3−/ Nm ratios in SecF can be interpreted as soil recovery, and that they reveal an efficient response to restoration by enhancing the N available to plants that, in turn, can reduce carbon loss (CO2 fluxes) from the soil. Our study showed high rate constants of C mineralization, representing high vulnerability to C loss. The narrow range of C mineralization rate constants obtained through the model suggests that mineralized organic compounds are relatively similar in terms of availability. In this study, variations in the percentage of Cm/ Nm ratios indicated that TSdF (1.94%) and SecF (2.0%) were more favorable for C stock accumulation, while DS_C (6.4%) and DS_S (4.6%) were sensitive to N immobilization. Data showed both negative (soil bulk density, soil hydraulic conductivity, C:N ratio, pH) and positive (soil availability water, soil organic nitrogen, soil organic carbon, cation exchange capacity) effects of soil properties on Co and No, all of which contribute to regulating SOM mineralization and C sequestration as well as the availability of N for soil microbial biomass and vegetation growth. There is strong evidence that forest restoration (SecF site) from ex-grasslands can lead to SOC preservation and sequestration and can also improve the N supply which, in turn, can contribute to stabilizing the carbon cycle at a regional scale.

(k) and C:N ratio (Fig. 7): as the C:N ratio increased, the N mineralization rate greatly decreased. This pattern is consistent with results published by Enríquez et al. (1993), who documented a negative relationship between N mineralization rate and C:N ratio. Our results highlight the importance of the nutritional balance (e.g. C:N ratio) of SOM in regulating N mineralization in sandy soils. In natural ecosystems, the C:N ratios of SOM inputs from litter and root exudates regulate soil microbial activity and nutrient availability (Drake et al., 2013). Therefore, the C:N ratio may be a good predictor of the quality and vulnerability of SOM in the sandy soils of tropical dry coastal ecosystems. SOM quality refers to how easily the carbon in soil organic matter can be mineralized (Bosatta and Ågren, 1999), thereby exerting an important influence on the N available for plant growth. Soil pH is one of the major factors affecting soil processes and properties. Our results showed that potentially mineralized N increased with decreasing soil pH throughout the study sites (Fig. 7), likely due to differences in organic matter content. This means that microbial activity might be stimulated under conditions of lower soil pH (e.g. < 7.0) in our case study. The lower pH noted in our study may be due to the mineralization of SOM, which releases weak organic acids (Murphy, 2015); this would indicate the buffering capacity of soil organic matter. Conversely, the higher soil pH may be due to lower SOM. A recent study (Cheng et al., 2013) reported that net N mineralization rates decreased with lower pH in forest soil. Thus, during microbially mediated processes, soil pH may strongly influence potentially mineralized N (Cheng et al., 2013). Such results imply that the N supply in the soils studied is vulnerable to the increasing pH that results from a reduction in SOM due to anthropogenic ecosystem disturbance relating to deforestation.

Acknowledgments 4. Conclusions Our thanks to the Consejo Nacional de Ciencia y Tecnología (CONACYT, Mexico), which funded this study through Project #CB2010/152457. We are also grateful to Lourdes Cruz Huerta for overseeing the incubation experiment, as well as to Sandra Rocha and Ninfa Portilla for their extremely valuable laboratory assistance. We are grateful to Rosario Landgrave for providing the location map of the study area. Special thanks go out to Eduardo Sáinz Hernández for providing daily climate data from CONAGUA's #30353 meteorological station.

The soil in these ecosystems contains more than 84% sand and less than 6.2% clay. The cation exchange capacity (CEC) is low, less than 17.8 cmol kg−1. Measurements of carbon and nitrogen mineralization can aid our understanding of soil functions and the effects of land use and climate change on soil organic matter. Short-term laboratory incubation experiments allow us to evaluate the state of vulnerability of soil organic matter to degradation in sandy soils, a change that results from modifications in land cover. The results presented herein highlight the potential of organic matter inputs relative to TSdF and SecF to preserve and restore C in soil, respectively. This could be attributed to 11

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