Influence of soil nutrients on net primary productivity in post-mining forests in the Colombian Pacific

: Tropical forests have the highest rates of net primary productivity (NPP) in terrestrial ecosystems and, therefore, may contribute significantly to the mitigation of global climate change. Although NPP is influenced by soil fertility, and recently, in some regions, mining activity in forest ecosystems has intensified. Little is known about how soils determine the restoration of NPP in forests degraded by mining. We evaluated the influence of soil nutrients on wood NPP of post-mining forests in the biogeographic Chocó region (Colombia), with emphasis on the effects of nitrogen (N) and phosphorus (P) limitations in post-mining forests under successional stages of 12-15 or 30-35 years. For this, permanent plots were established in secondary post-mining forests in Jigualito (Colombian Pacific), the wood NPP (accumulated and current) was evaluated, and it was related to soil properties such as organic matter (OM), acidity, Al, total N, available P, magnesium (Mg), potassium (K), calcium (Ca), and texture. An accumulated wood NPP of 0.72 t ha -1 yr -1 was recorded in post-mining forests 12-15 years old. Meanwhile, in post-mining forests of 30-35 years, the accumulated wood NPP was 6.52 t ha -1 yr -1 . The current wood NPP was 4.25 t ha -1 yr -1 in post-mining forests with 30-35 years of recovery. Accumulated NPP positively correlated with soil OM, total N, Ca, Mg, and effective cation exchange capacity–ECEC in post-mining forests. In post-mining forests, a slow recovery of the wood NPP was denoted in the first years. Soil nutrients determined the wood NPP, and a multiple limitation of nutrients with the succession was observed, which corroborates the need to restore the degraded ecosystem in the region.


INTRODUCTION
Tropical forests are considered the most important terrestrial ecosystem in terms of net primary productivity (NPP) and have a key role as sinks and reservoirs of atmospheric carbon (Phillips et al., 1998;Clark et al., 2001b;Grace, 2004;Pan et al., 2011).Specifically, it has been estimated that these forests store about 40 % of the existing carbon in the terrestrial ecosystems of the planet (Dixon et al., 1994), they represent 36 % of the global NPP (Field et al., 1998;Beer et al., 2010) and capture about 1.19 petagrams of carbon annually (Pg C yr -1 ) (Pan et al., 2011), thus contributing significantly to carbon fixation and balance, and global climate change mitigation (Grace, 2004;IPCC, 2014).Consequently, there is a growing interest in evaluating the NPP of these forests, and the environmental and anthropic factors that determine it (Phillips et al., 1998;Clark et al., 2001a;Malhi et al., 2004;IPCC, 2014).
Several studies have documented that the NPP of tropical forests is influenced by factors such as precipitation, climate, solar radiation, temperature, soil type and its fertility, as well as by other factors related to the dynamics (disturbances) of the ecosystem, structure and species composition (Schuur, 2003;Del Grosso et al., 2008, Jiménez et al., 2009;Cleveland et al., 2011;Malhi et al., 2011;Wu et al., 2011;van der Sande et al., 2018;Linger et al., 2020); for this reason, a wide range of aboveground NPP has been shown in tropical rainforests, between 1.2 and 15.2 Mg ha -1 yr -1 (Clark et al., 2001b).
Soil nutrient content has shown a positive effect on NPP of tropical forests (Alvarado and Raigosa, 2012;van der Sande et al., 2018).In this sense, it has been determined nutrients tend to be more correlated with NPP are N, P, K and Ca (Paoli and Curran, 2007;Cleveland et al., 2011); which are part of the nutrients considered physiologically essential for plant growth (Lambers et al., 2008a).For example, Vitousek (1984) conducted an analysis of N, P and Ca recycling and determined the availability of P, but not N, limited the litter production (a component of the NPP).Meanwhile, Paoli and Curran (2007) observed that the NPP of tropical forests increased with the availability of P, N, K, Ca, Mg, and ECEC.Similarly, Aragão et al. (2009) reported Amazon's NPP (total and fine roots) increases significantly with the P content of the soil.Likewise, some years ago, in a meta-analysis on NPP in tropical forests, Cleveland et al. (2011) reported P availability positively influences the NPP rates.On the other hand, Quinto et al. (2017) observed that the production of leaves and fine roots increased with soil fertility in forests of the biogeographic Chocó.In summary, these studies show the importance of soil nutrients on NPP and mitigating global climate change.
However, in recent decades, tropical forests have been severely deforested and degraded due to human activities such as logging, agriculture, cattle ranching, and mining, among others (Primack, 2008), which affect the ability of these ecosystems to mitigate global climate change (Grace, 2004;IPCC, 2014).Particularly, open-pit mining strongly impacts the NPP, once vegetation and soil covers are removed (Diaz and Elcoro, 2009;Valois, 2016;Maus et al., 2022;Giljum et al., 2022).Not only soil and vegetation are affected, but all the ecological processes of the ecosystem (Holl, 2002;ELAW, 2010).In this sense, with mining, there is a reduction in the capture of atmospheric CO 2 due to the loss of vegetation, the carbon balance is altered, and CO 2 emissions into the atmosphere increase, which accentuates global warming (ELAW, 2010).It is estimated that from 2001 to 2013, about 1680 km 2 of South American tropical forests were lost (Primack and Vidal, 2019), with threatening effects not only to the region's biodiversity, but also to soil organic carbon (SOC) and to the capacity of ecosystems to mitigate global climate change.
This situation is currently taking place in Colombia, in the Chocó (Colombian Pacific) department, where open-pit gold mining is damaging soil and rivers of the natural ecosystems (Valois, 2016).Nonetheless, about 840 thousand hectares of mature forest were recently granted licenses for mining exploitation in the territory (Ángel et al., 2019).Now, it is necessary to develop restoration projects and programs to recover the functionality and NPP of the ecosystem.Knowing the environmental factors that limit the NPP of post-mining ecosystems is necessary to achieve this purpose.
Rev Bras Cienc Solo 2024;48:e0230053 In this sense, Kalamandeen et al. (2020) reported an increase in NPP of post-mining forests in the Amazon, in areas where soil had higher N content, denoting the influence of soil nutrients on the restoration of degraded ecosystems.Likewise, it has been hypothesized that, in tropical soils, in initial successional stages, there is a limitation of the NPP by N, which over time is mitigated due to colonization of plants with capacity to fix atmospheric N 2 symbiotically (Walker, 1993).Therefore, in the ecosystem, to the extent that there is a greater colonization of N-fixing plants, and succession advances, this limitation of the NPP would be reduced (Cleveland et al., 1999;Walker and del Moral, 2008).Unlike N, the levels of soil P tend to be high in the first successional stages, and over time, its availability to plants tends to decrease due to losses by leaching and immobilization in Fe and Al oxides (Walker and Syers, 1976;Vitousek et al., 2010).With this, a limitation of the NPP is expected due to low availability of P in advanced successions and mature forests (Vitousek, 1984).
Based on the above discussion and taking into account that the region is one of the most biodiverse on the planet (Rangel, 2004), and has one of the highest levels of precipitation (Poveda et al., 2004); that possibly affects the edaphic limitation and availability of nutrients due to leaching (Austin and Vitousek, 1998;Posada and Schuur, 2011;Quinto and Moreno, 2016); this study aimed to evaluate the soil nutrients influence on the wood NPP of post-mining forests in the biogeographic Chocó, and, contribute with experimental elements to the restoration of the NPP of these degraded ecosystems.

Study area
This study was carried out in forested areas previously degraded by open-pit gold mining, in the locality of Jigualito (5° 06' 01" N -76° 32' 44" W), in the municipality of Condoto, department of Chocó, Colombia.Average annual precipitation is 8000 mm, the mean annual temperature is 26 °C, and altitude is 70 m with flat topography.This locality is part of the biogeographic subregion of North Central Chocó, which includes the upper basins of the Atrato and San Juan rivers, in Piedemonte and Colinas lowland landscape units with humid soils and a type of transitional sedimentary rock (Poveda et al., 2004).The localities lie within the Tertiary Sedimentary Hills geomorphological unit formed by low-altitude sedimentary rocks composed of sandy clayey, sandstone and limestone.The forests are mostly secondary, with different recovery ages since mining has been carried out in the area at different times.
Soils of the post-mining forests are Alisols (WRB) or Ultisols (Soil Taxonomy) and, due to mining, they have rocky material and sand.The A horizon was removed during mining, with irregular return of organic material after mining.In addition, they are acidic and have high OM, total N, available P, Al and clay contents; while the contents of Ca, K, Mg, ECEC and silt are low (Quinto et al., 2022).In these forests, the most dominant tree species are Cecropia peltata, Vismia baccifera, Cosmibuena macrocarpa, Ochroma pyramidalis, Welfia regia, Pityrogramma calomelanos, Cespedesia spathulata, Inga chocoensis, and Pourouma bicolor (Ramírez and Rangel, 2019).
This study assessed two post-mining forests with different succession times.These forests were secondary forests that grew in abandoned illegal mining areas.The first post-mining forest was 12-15 years old (F12-15) and the second forest was 30-35 years old (F30-35), being that the time of restoration after mining ended.In the post-mining forests F12-15, 103 plots of 5 × 5 m (25 m 2 ) were installed as NPP sampling units; while in the forests F30-35, 37 plots of 10 × 10 m (100 m 2 ) were installed.Plot size and replicates in each forest were different due to irregular site characteristics, which only allowed sampling in this way.

Physical and chemical soil properties
In each plot (103 and 37 in the post-mining forest of 12-15 and 30-35 years, respectivity), composite samples of soil were taken at a depth of 0.20 m, to which the parameters of acidity (pH), aluminum content (Al ), organic matter (OM), total N, available P, calcium (Ca), potassium (K), magnesium (Mg), effective cation exchange capacity (ECEC), and texture (percentages of sand, silt, and clay), according to the following laboratory techniques: Bouyoucos for textural fractions, potentiometric in water solution (1:2) for pH, Walkley and Black for OM, Micro-Kjeldahl for total N, ascorbic acid in an UV-VIS spectrophotometer after extraction with the Bray II method for available P, atomic absorption for Ca, Mg, and K extracted with ammonium acetate, described in Osorio (2014), andQuinto et al. (2022).Soil sampling was carried out in 2020 and 2021.

Diameters and height of trees
In the installed plots, the sampling criteria for the forest inventory was stratified sampling by succession time forests; here the circumference at breast height (1.30 m above ground level) was measured with a measuring tape in all trees with circumference >31.4 cm (Diameter at breast height-DBH >10 cm) in each quadrat; subsequently, the circumference values were transformed to DBH.The perimeter of the tree trunk where the DBH was measured was marked with yellow paint to ensure that subsequent measurements were made in the same strip as the first measurement.Measurement of tree heights was carried out with a Clinometer at fixed distances of 15 m from the tree.All measured trees were marked with aluminum plates.Additionally, growth habits were identified, and the characteristics of each individual were recorded.Trees were measured each August of 2020, 2021 and 2022 in F30-35; while in F12-15, inventories were carried out only in 2020 due to armed conflicts in the area.In total, 114 trees were excluded from the analysis because they died during the sampling period.

Botanical identification
Trees were identified at the highest possible taxonomic level (species, genus, botanical family) in the herbarium of the Technological University of Chocó "Herbario Chocó".This identification was made using the specialized key of Gentry (1993), and the scientific names of species and families were corroborated on the "Tropicos" website.(https://www.tropicos.org/home).This taxonomic information was used to determine the wood density.

Wood density
We used values published in two international databases of wood density obtained for tropical forests (Brown, 1997;Baker et al., 2004).In case a species or genus found in the plots was not reported in these databases, the average of the genus or family of the species was used.

Aboveground biomass and wood net primary productivity (wood NPP)
The allometric model proposed by Álvarez et al. (2012) (Equations 1, 2 and 3), based on data from the same region, was used to determine the trees' aboveground biomass (AB).
Eq. 1 Current wood NPP = (final AB -initial AB)/ time in years Eq. 2 Accumulated wood NPP = AB/the succession time in years Eq. 3 Rev Bras Cienc Solo 2024;48:e0230053 in which: AB is the aboveground biomass in kilograms; DBH is the diameter in cm; H is the height of the tree in m; ln is the natural logarithm; and ρ is the wood density.Aboveground biomass was determined at the ecosystem, species, and tree individual levels.The AB was estimated by applying harvest-based allometric regression equations to measurements of the diameters of all trees in a plot that are above the minimum size, and was expressed in tons per hectare (Mg ha -1 ) (Clark et al., 2001a).Current wood NPP (2) was estimated from two successive stand-level AB estimates; that is to say, the annual increment of the AB was used, which was determined as the final AB of the trees, minus the initial AB, divided by time in years (Clark et al., 2001a).These determination of the Current wood NPP could only be carried out in F30-35.Meanwhile, the Accumulated wood NPP (3) was calculated as the AB divided by the succession time, in years (Silver et al., 2000).Wood NPP values were expressed in tons per hectare per year (Mg ha -1 yr -1 ) (Clark et al., 2001a).The NPP includes not only the growth of primary producers (biomass accumulation and tissue turnover above and belowground in terrestrial ecosystems) but also the C transfer to herbivores and root symbionts (for example, mycorrhizal fungi), the excretion of organic C from algae, and the production of root exudates and plant volatile organic compounds (VOCs) (Clark et al., 2001a).

Statistical analysis
Assumptions of normality and homogeneity of variances were first evaluated with Bartlett, Hartley and Kurtosis statistical tests (between + 2.0 and -2.0).Data distribution was evaluated for each treatment using the Shapiro-Wills statistical test.Initially, mean values of wood NPP between post-mining forests (12-15 years vs 30-35 years) was compared with the Mann-Whitney (MW) test because the data did not meet the normality assumption and did not present a normal distribution (Hoshmand, 1998).The wood NPP and soil data were log-transformed whenever possible to achieve a normal distribution.Subsequently, to determine the relationship between wood NPP and soil physical and chemical properties, General Linear Models (GLM) with mixed effects, Spearman rank correlation analysis, and linear regression models (Hoshmand, 1998) were used.Spearman analyses were performed for each of the post-mining forests, and then the two post-mining forests were taken as a single ecosystem.Meanwhile, the General Linear Models (GLM) and the Linear Regression Models were carried out taking the post-mining forests as a single forest ecosystem, due to the geographic proximity and the floristic and structural similarity (Ramírez and Rangel, 2019).Analyses were performed in the R programming environment (R Development Core Team, 2013).
On the other hand, when evaluating the post-mining forests as a single ecosystem, it was denoted by the GLM that OM, Ca, and Mg contents were significantly related to the accumulated wood NPP, and those soil properties explained 40.6 % of its variation (R 2 = 40.6 %) (table 2).For its part, Spearman's correlation showed that the accumulated wood NPP was positively and significantly related to Al, OM, total N, available P, Ca, Mg, and ECEC; while, with pH and clay, the relationship was negative (Table 3).Likewise, it was noted that the accumulated wood NPP presented the highest correlations with OM (R 2 = 25 %), Ca (R 2 = 23 %), Mg (R 2 = 14.4 %), total N (R 2 =11.4 %), and ECEC (R 2 = 23 %) (Figure 1).
Finally, a very weak negative correlation with Mg was evidenced when evaluating the wood NPP of post-mining forests with 12-15 years of recovery (Table 3).Meanwhile, the accumulated wood NPP of 30-35 years post-mining forests showed a negative correlation with the total N (Table 3).For its part, the current wood NPP of post-mining forests of 30-35 years of recovery showed a negative and not significant correlation with sand, but, positive and also insignificant with silt and clay (Table 3).

Carbon sequestration in post-mining secondary forests
Wood NPP of post-mining secondary forests in the Colombian Pacific was between 0.01 and 9.82 Mg ha -1 yr -1 , with an average of 0.75 Mg ha -1 yr -1 in areas with ages between 12-15 years.Those figures are partially similar to those of 0.70-9.15Mg ha -1 yr -1 reported for secondary post-mining forests in Cértegui (Chocó, Colombia), with an average of 3.51 Mg ha -1 yr -1 in areas between 1.5 and 6.0 years of restoration (Quinto et al., 2013).Likewise, such wood NPP was similar to the 0.4-5.4Mg ha -1 yr -1 reported for 3-4 years forest succession in abandoned mining areas in the Amazon (Kalamandeen et al., 2020).Therefore, it seems wood NPP of post-mining forests with less than 20 years of recovery, in the Colombian Pacific and in the Amazon (Quinto et al., 2013;Kalamandeen et al., 2020) are within the range of 0.01 to 32.7 Mg ha -1 yr -1 reported for Neotropical secondary forests (Poorter et al., 2016).
However, the 0.75 Mg ha -1 yr -1 of NPP in recent post-mining areas (12-15 years of restoration) is much lower than that of the majority of secondary tropical forests (of approximately 6.1 Mg ha -1 yr -1 ) after the abandonment of activities such as cattle ranching, agriculture and logging (Silver et al., 2000;Poorter et al., 2016).For example, in the central Amazon, a wood NPP rate of 11.0 Mg ha -1 yr -1 was recorded for 14 years of recovery after the abandonment of grazing (Feldpausch et al., 2004).Likewise, in secondary forests with ten years of recovery, 5.5 Mg ha -1 yr -1 of wood NPP was obtained in another ecosystem of the same Amazonian macro-basin (Johnson et al., 2000).Those results show the influence of the type of the previous disturbance on the recovery capacity of the ecosystem (Silver et al., 2000;Guariguata and Ostertag, 2001;Chazdon et al., 2016).Specifically, it is corroborated that open-cast mining significantly affects the ecosystem, which generates a slow biomass recovery and functionality, as has been suggested in previous analyses of tropical successions (Guariguata and Ostertag, 2001).
Wood NPP of recent post-mining forests (<20 years) is low is probably due to the impact that mining has on the ecosystem.Soil organic horizon is removed, and the overall soil structure is altered, mainly leaving rocks and sand on the surface (Ramírez et al., 2019).Vegetation and the soil/regolith that covers mineral deposits are removed (Diaz and Elcoro, 2009;Valois, 2016), affecting soil fertility (Quinto et al., 2022), plant biomass (Quinto et al., 2013) and many other ecological processes (Holl, 2002;ELAW, 2010), like nutrient recycling (Quinto et al., 2022) and carbon sequestration (NPP) (Kalamandeen et al., 2020).Such effects are stronger than those generated by other anthropic activities like selective felling of trees, subsistence agriculture, and grazing (Silver et al., 2000), which still preserve the organic horizon, texture, and soil nutrients (Guariguata and Ostertag, 2001).
On the other hand, the post-mining forests between 30-35 years of recovery had average wood NPP of 4.25 and 6.52 Mg ha -1 yr -1 , comparable to the report of 6.1 Mg ha -1 yr -1 for Neotropical secondary forests (Silver et al., 2000;Poorter et al., 2016), or higher than reports of 1.01 to 4.36 Mg ha -1 yr -1 for secondary rainforests between 23 and 40 years of recovery after logging in the biogeographic Chocó (Forero-Peña et al., 2022).Possibly, this increase in the wood NPP of the post-mining areas with the regeneration age is due to the increase in the edaphic content of OM and nutrients (total N, Ca, Mg, ECEC) that occurs with the succession (Quinto et al., 2022).Likewise, over the succession, there is an increase in activity, abundance, functionality (ammonification and nitrification), richness and post-mining microbial biomass (Sansupa et al., 2021).In addition, the edaphic colonization of mycorrhizae may increase (Zhang et al., 2017).In early succession Rev Bras Cienc Solo 2024;48:e0230053 ecosystems (<20 years), the presence of mycorrhizae is low.In contrast, in post-mining forests with a longer recovery time, such as in mines >30 years of abandonment, surely the presence of arbuscular mycorrhizae and edaphic proteins related to glomalin favor recalcitrant carbon components, which benefit the accumulation of soil organic carbon (SOC) and OM in tropical forests (Zhang et al., 2017).This surely explains the higher wood NPP in these advanced succession post-mining forests.
Another factor that explains the higher wood NPP of advanced succession post-mining forests (>30 years) in the Colombian Pacific is the colonization by tree species, either pioneer or climax, that store greater amounts of carbon in a shorter time (Guariguata and Ostertag, 2001).The composition of tree species recorded in these abandoned mines were Cecropia peltata, Vismia baccifera, Cosmibuena macrocarpa, Ochroma pyramidalis, Welfia regia, Pityrogramma calomelanos, Cespedesia spathulata, Inga chocoensis, and Pourouma bicolor) (Ramírez and Rangel, 2019).Those species have been commonly reported for previously degraded ecosystems, secondary forests and areas with different stages of ecological succession (Alves et al., 1997;Guariguata and Ostertag, 2001).These species are possibly the ones with the greatest tolerance to adverse conditions (isolation, high temperatures, stress, acidity, herbivory, infertility and Al toxicity) that occur in areas degraded by mining (Diaz and Elcoro, 2009;Valois, 2016;Quinto et al., 2022).For this reason, it can be deduced that this physiological capacity contributes significantly to the wood NPP of the previously degraded ecosystem.

What influences do soil nutrient contents have on wood NPP of post-mining forests of the biogeographical region of Chocó?
Soil conditions were essential for the restoration of the wood aboveground biomass (wood AB) and wood NPP in abandoned mines in tropical regions (León and Osorio, 2014).However, in our study, the current wood NPP (Clark et al., 2001b) did not show a significant relationship with soil nutrient content variations; similar to what was observed by Oberleitner et al. (2021) in measurements of an increase in wood AB in secondary forests of Costa Rica.Likewise, Poorter et al. (2016) recorded only a significant association between the accumulation of wood AB and ECEC in tropical secondary forests.For this reason, annual changes in wood NPP of the trees could have little relationship with the spatial variation in the contents of soil nutrients.This is surely due to the fact that most trees growing on acidic and nutrient-poor soils are adapted to low nutrient availability (Whitmore, 1998;Lambers et al., 2008b), and changes in their availability generate responses.In the long term, which is not easily evidenced from one year to the next, as has happened in some studies when the tree wood NPP is evaluated in annual inventories (Aragão et al., 2009;Cleveland et al., 2011;Quinto and Moreno, 2017;Oberleitner et al., 2021); as it happens in this study carried out in post-mining forests.
On the other hand, in the accumulated wood NPP, calculated as the wood AB divided by the succession age in years (Silver et al., 2000), a positive relationship was evidenced between the wood NPP and soil nutrients (OM, total N, Ca, Mg, and ECEC) in postmining forests, which together show that small soil patches of higher fertility tend to facilitate carbon accumulation and the recovery of ecosystem functionality.Such wood NPP rate observed in more fertile soils of abandoned mines is similar to that reported by Kalamandeen et al. (2020), who reported a higher wood NPP in abandoned mines with higher total N content.Likewise, Poorter et al. (2016) determined that the percentage of AB accumulation is determined by soil fertility (CEC) in Neotropical secondary forests in different successional stages.Likewise, Tucker et al. (1998), in secondary forests with more than 15 years of succession, compared the recovery of the basal area (indirect measure of the forest biomass) in fertile and nutrient-rich soils, with the recovery on infertile soils, Oxisols; and found that in fertile soils the basal area was much greater over the succession time, and in such forest, the AB of a primary forest was reached more quickly (Tucker et al., 1998).Thus, the positive influence of edaphic fertility on wood NPP Rev Bras Cienc Solo 2024;48:e0230053 in tropical forests is evidenced (Moran et al., 2000;Guariguata and Ostertag, 2001;Lu et al., 2002) at local and regional scales, as occurs in areas previously degraded by open pit mining.Meanwhile, Feldpausch et al. (2004) recorded a higher accumulation of AB and wood NPP in secondary forests (12-14 years of recovery) of the Amazon in areas with higher edaphic content of total N.This evidences the strong influence of soil nutrients on the wood NPP of tropical secondary forests, including those generated by mining.
It is important to mention that, although some studies have not shown a significant relationship between soil nutrients and AB accumulation in tropical secondary forests (Poorter et al., 2016;Oberleitner et al., 2021), fertilization experiments developed to evaluate the nutritional limitation of wood NPP in secondary forests, have had different revealing results (Vitousek and Farrington, 1997;Harrington et al., 2001;Davidson et al., 2004).For example, Harrington et al. (2001) reported higher wood NPP with N and P application in secondary forests limited by N (young secondary forest) and P (old secondary forest), respectively.Likewise, Campo and Vázquez-Yanes ( 2004) observed a greater litter production (NPP component) with the application of N+P in young (10 years) and old (60 years) secondary dry forests, respectively.Similarly, Davidson et al. (2004) recorded a higher wood NPP with the application of N and N+P in six-year-old secondary forests in the Amazon.These experiments show the limitation of N in early successional stages (Davidson et al., 2004) and the restriction of P in late successional stages (Harrington et al., 2001).Likewise, these results show the influence of different soil nutrients on the wood NPP in successional processes, which denotes a multiple nutritional limitation (Kaspari et al., 2008;Sullivan et al., 2014), as could be asserted in the present study.
The fact of registering a higher wood NPP in post-mining forests with high OM and total N contents is similar to that reported in secondary forests of the Amazon, where a higher wood carbon capture was observed in forests with higher total N in the soil (Feldpausch et al., 2004;Kalamandeen et al., 2020).In particular, the fact that wood NPP increases with total N is crucial, because this nutrient is considered one of the limiting factors for plant growth (Lambers et al., 2008a) and NPP of primary tropical forests (Paoli and Curran, 2007;LeBauer and Treseder, 2008;Quinto and Moreno, 2017) and secondary (Feldpausch et al., 2004;Kalamandeen et al., 2020).Total N is fundamental to photosynthesis, formation of ATP and NADPH+ molecules, and in the constitution of chlorophyll (Lambers et al., 2008a); therefore, it is fundamental for the wood NPP of the post-mining forests of the Colombian Pacific.Likewise, the influence of other nutrients (Ca, Mg and ECEC) on the wood NPP, denotes a limitation due to multiple nutrients (Paoli and Curran, 2007;Kaspari et al., 2008), which shows the need to develop active restorations, applying various nutrients in abandoned mines.
A particular aspect observed in the present investigation was wood NPP did not present a significant relationship with the availability of edaphic P in post-mining forests; which is contrary to what has been reported in old secondary forests (Vitousek and Farrington, 1997;Harrington et al., 2001), and in mature tropical forests (Cleveland et al., 2011), such as those of the Amazon (Aragão et al., 2009), Indonesia (Paoli and Curran, 2007) and the biogeographic Chocó (Quinto et al., 2017).Possibly, the little relationship registered between the wood NPP and the P available in post-mining forests is due to reasons such as: 1) the little variation registered in the P available from the post-mining soil, since with mining and the subsequent succession edaphic always presented high values (P available = 26.02vs 32.09 ppm) (Quinto et al., 2022), with which, there was no true deficiency gradient in the soil; 2) the adaptive strategies developed to acquire edaphic P, such as mycorrhizal associations and the growth of a "cluster" network of fine roots that extract the P present in insoluble inorganic phosphates in the soil (Lambers et al., 2008b); with which, the wood NPP rates tend to be similar and make it difficult to show relationships with the P available from the soil.
Rev Bras Cienc Solo 2024;48:e0230053 Could it be that there are limitations of the wood NPP due to the availability of soil nutrients (N and P) in post-mining forests, as suggested by the published hypotheses (Vitousek, 1984;Lambers et al., 2008b;Kalamandeen et al., 2020)?
The hypothesis of nutritional limitation of the wood NPP of the forest has been raised by soil P availability and total N with the succession (Walker and Syers, 1976); according to which, in tropical soils with initial successional ages, there is little availability of N, due to its reduced biological fixation and scarcity of leguminous plants (Walker, 1993;Davidson et al., 2004).However, to the extent that there is a greater colonization of N-fixing plants, the biomass of the ecosystem increases and the succession advances, its availability increases, and this limitation is reduced (Cleveland et al., 1999;Walker and del Moral, 2008).Whereas, the levels of P in the soil tend to be high in the first successional stages, and over time its availability tends to decrease and be limited in the ecosystem (Vitousek et al., 2010), due to losses by leaching and immobilization in Fe and Al oxides, especially in tropical clayey soils (Walker and Syers, 1976;Vitousek et al., 1993;Reed et al., 2011).
This hypothesis was partially corroborated in the present investigation, given it was observed wood NPP and the total N are positively correlated in post-mining forests; as has been proposed for secondary forests (Vitousek and Farrington, 1997;Harrington et al., 2001;Davidson et al., 2004;Feldpausch et al., 2004); while there was no significant correlation with the available P content.Which is similar to what has been recorded in other investigations (Feldpausch et al., 2004).However, in the post-mining forests, there was also a correlation between the wood NPP and the OM, Ca and Mg contents of the soil; which shows that, in initial stages of the succession, not only can there be a limitation by total N (Kalamandeen et al., 2020), but also, there is a limitation by multiple soil nutrients, in areas previously degraded by mining.

CONCLUSIONS
In post-mining forests, soil nutrients determined the wood NPP, and multiple limitations of nutrients with the succession were observed, corroborating the need to restore the degraded ecosystem.The rates of carbon sequestration reported in post-mining forests in the Colombian Pacific denote the degradation of the functioning of the ecosystem generated by mining and reveal its negative influence on the role of these ecosystems in the carbon balance and in mitigating global climate change.The first years of postmining forest recovery, when less carbon sequestration and greater damage to the ecosystem is evident compared to other anthropic activities such as agriculture and livestock, show the need to develop restoration processes after mining.
Likewise, the fact that post-mining forests present high rates of wood NPP and carbon sequestration after a few decades of deforestation and mining is an opportunity for the development of reforestation programs of forests, which allow the mitigation of global climate change and the conservation of the Colombian Pacific region.

Table 1 .
Aboveground biomass and wood net primary productivity of two post-minigng forests in the Colombian Pacific NPP is the net primary productivity in tons per hectare per year (t ha -1 yr -1 ), the letters a and b indicate significant differences between the medians.Asterisks indicate statistically significant differences *: p<0.05; **: p<0.01; ***: p<0.001.SE is the standard error.

Table 2 .
Analysis of variance of wood net primary productivity based on the soil physicochemical properties Statistical method was General Linear Model.R 2 = 40.6 %.Rev Bras Cienc Solo 2024;48:e0230053

Table 3 .
Spearman correlations of carbon sequestration and physicochemical properties of post-mining forests in the Colombian Pacific