Selection of forest species for the rehabilitation of disturbed soils in oil fields in the Ecuadorian Amazon

Science of the Total Environment 566–567 (2016) 761–770

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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Selection of forest species for the rehabilitation of disturbed soils in oil fields in the Ecuadorian Amazon Jaime Villacís a,c,⁎, Fernando Casanoves b, Susana Hang c, Saskia Keesstra d, Cristina Armas e a

Departamento de Ciencias de la Vida, Universidad de las Fuerzas Armadas (ESPE), Av. General Rumiñahui s/n, Sangolquí, P.O.BOX: 171-5-231B, Ecuador Biometric Unit, Tropical Agricultural Research and Higher Education Center (CATIE), Turrialba, Costa Rica Facultad de Ciencias Agropecuarias, Universidad Nacional de Córdoba, CC 509, 5000 Córdoba, Argentina d Soil Physics and Land Management Group, Wageningen University, Droevendaalsesteeg 4, 6708, PB, Wageningen, The Netherlands e Estación Experimental de Zonas Áridas, CSIC, Almería, Spain b c

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• Petroleum activities may cause severe soil erosion. • Plants of 20 species were planted in disturbed soils in oil fields in the Amazon. • We measured plant performance and changes in soil characteristics after two years. • Trees decrease hydrocarbons levels between 11 to 22 % in contaminated soils. • Five species are the most suitable for restoration of oil fields in Amazon Basin

a r t i c l e

i n f o

Article history: Received 22 March 2016 Received in revised form 14 May 2016 Accepted 15 May 2016 Available online xxxx Editor: Jay Gan Keywords: Hydrocarbon contaminated soils Forest restoration Rehabilitation of oil fields Sapling performance Ecuadorian Amazon

⁎ Corresponding author. E-mail address: [email protected] (J. Villacís).

http://dx.doi.org/10.1016/j.scitotenv.2016.05.102 0048-9697/© 2016 Elsevier B.V. All rights reserved.

a b s t r a c t Soils in the Amazon Basin disturbed by petroleum extraction activities need to be restored to allow for the rehabilitation of these areas and the restoration of the ecosystem services that these areas can provide. This study explores the performance of saplings of 20 species transplanted to four sites: a paddock and three sites within oil fields that differ in soil substrate contamination and perturbation. In each site we measured sapling survival, possible causes of death, sapling height and diameter at the time of and two years after planting, and the integrated response index. We also analyzed the effects of plants on soil properties. Sapling mortality was limited, with 17 of the 20 species boasting survival rates of over 80%. Saplings in the control site had a higher mortality rate than those in the oil field sites. This was most likely due to competition with and interference of weeds that were more abundant at the control than other sites. Despite the overall low mortality rate, species performance did vary by site, with plants of Flemingia macrophylla, Myrcia aff. fallax, Piptadenia pteroclada, Platymiscium pinnatum, and Zygia longifolia exhibiting the best performance in terms of survival and growth in oil field sites. At the end of the experiment, soil substrates from the oil platform showed increases in pH levels, organic material, Fe, and Zn; whereas substrates contaminated with petroleum showed decreases in hydrocarbon levels ranging from 11 to 22% compared to initial levels before planting. Our results shed light on which forest species are most suitable

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for the rehabilitation of sites disturbed by activities inherently associated with petroleum extraction in the Ecuadorian Amazon. © 2016 Elsevier B.V. All rights reserved.

1. Introduction The degradation of soil and reduction of vegetation cover caused by human activity are increasing globally as a consequence of agriculture, grazing, mining and urban developments (Bruun et al., 2015; Ferreira de Araújo et al., 2015; Ochoa et al., 2016; Russell and Ward, 2016). The loss of soil quality causes a loss in soil functional activities, and this results in the loss of the ecosystem services, resources and goods that these soils offer to humankind; these in turn have important negative effects on the geochemical, hydrological, and biological Earth System cycles (Berendse et al., 2015; Brevik et al., 2015; Decock et al., 2015; Smith et al., 2015; Keesstra et al., 2016). The oil industry constitutes one of the largest and most lucrative industrial activities on the planet, as petroleum is one of humanity's main sources of energy (Pérez-Hernández et al., 2013). However, the increase in hydrocarbon extraction activities in continental regions results in the degradation and erosion of vast territories (Namkoonga et al., 2002), thereby creating one of the most severe environmental problems in the world (Übelhör et al., 2014). Soil degradation is one of the most negative impacts of the activities inherent to petroleum extraction (Orta Martínez et al., 2007). It is caused by the removal of plant cover and upper soil layers during the construction of drilling platforms, as well as by the contamination of soils with hydrocarbons, heavy metals, and other chemical substances that are stored as byproducts in mud and drill cutting cells and contaminated soil treatment units in the oil field facility (Willis et al., 2005). Moreover, the construction of drilling platforms is done using heavy machinery, which leads to soil compaction (Startsev and McNabb, 2000) and affects soil's physical properties (Håkansson and Reeder, 1994). In the Latin American region, countries such as Guatemala, Mexico, Peru, Bolivia, Nicaragua, Panama, and Ecuador are all carrying out petroleum extraction activities even in protected areas, threatening the natural heritage of the region with the highest level of biodiversity on the planet (Gentry, 1993). In Ecuador, petroleum is the main source of income, and it is essential to the country's economic development. Approximately 4.2 million ha — 15% of Ecuador's entire territory – are altered by petroleum extraction activities, and most of this area lies within Amazonian ecosystems. Consequently, oil field sites require rehabilitation to reduce both on-site effects (soil erosion, loss of soil fertility, and soil contamination) and off-site effects such as sediment accumulation in rivers and reservoirs (Jorgenson and Joyce, 1994). The sediment and water leaving the oil fields contains pollutants that may reach bodies of water downstream, further affecting natural resources and, potentially, human health (Ko and Day, 2004). Forest restoration activities are essential tools to rehabilitate degraded areas and to restore part of the form, functions and ecosystem services that these areas delivered before the human-induced land perturbation occurred (Hobbs and Harris, 2001). Restoration of the vegetation cover generally leads to improvements in soil properties (Fialho and Zinn, 2014; de Moraes Sá et al., 2015; Ochoa-Cueva et al., 2013), as has been previously demonstrated in Ecuador and other South American regions. After a few years of revegetation, organic matter increases and biological activity is stimulated (Jones et al., 2004), restoring the functions of the soil. Moreover, these enhanced soil properties and the plants growing in them can neutralize or stabilize the soil contaminants, potentially rendering them unavailable to other organisms (Merkl et al., 2004). A successful restoration process depends largely upon the selection of plant species and the ability of these to adapt to degraded soil conditions (Bradshaw and Huttl, 2001). At a global level, some studies have been carried out to select plant species for soils disturbed by petroleum

extraction activities, and to assess the effects of these species on soil characteristics in tropical and subtropical ecosystems (e.g., McConkey et al., 2012 and Willis et al., 2005 in America and Mohsenzadeh et al., 2010; Shirdam et al., 2008 and Xia, 2004 in Asia). However, as far as we know there are no such studies in the Amazon Basin. In the Ecuadorian Amazon, the reforestation projects in oil fields have mostly selected a combination of native and exotic species based on the knowledge of farmers and local technicians, rather than on any systematic study that determined species' suitability to restore these sites. Thus, these reforestation projects were largely unsuccessful, partly due to unknown plant performance, growth, or adaptability to the specific conditions of contaminated soils, and partly due to an inadequate control of weeds. This has led to low survival levels, and very poor species growth following transplanting (Villacís et al., 2016). The main objective of this study was to evaluate the performance of 20 tree species planted in areas disturbed by activities associated with petroleum extraction in Amazonian Ecuador. For the two years following their planting, we tested the performance of these trees on different sites: a paddock control site and three sites within the oil fields' facilities that differ in soil compaction and contamination. We also evaluated the effect of these plants on soil characteristics to assess whether the use of these species could feasibly be used as a tool to improve soil characteristics. We hypothesized that soil contamination by hydrocarbons and heavy metals in oil fields would have the worst impact on plant growth and survival irrespective of the species planted, while other soil physicochemical perturbations (soil compaction and clearance of the first soil horizon, the organic horizon) would have a lower impact on plant performance compared to plants growing in surrounding paddocks. Moreover, we expected that surviving plants would have a measurable effect on soil properties two years after planting. The ultimate goal of this study was to produce a list of species recommended for use in restoration projects of oil fields in the Amazonian Basin based on their abilities to survive, grow, and amend soils affected by oil extraction activities. 2. Materials and methods 2.1. Study site The study was performed in the Sucumbíos (0° 5′S, 76° 53′W) and Orellana (0° 56′S, 75° 40′W) provinces in the Ecuadorian Amazon (Fig. 1). Both provinces have an average altitude of 328 m, a mean annual precipitation of 3000 mm, a mean annual temperature of 25 °C, and a relative humidity of 85%. The area is classified as “tropical rainforest” (Peel et al., 2007). Soils in this area are typically acidic, and have low nutrient levels and high aluminum contents (Villacís et al., 2016); these singularities lead to rapid soil erosion and infertility after the vegetation is removed from the oil fields (Nichols et al., 2001). Taking into account the availability of sites located in the study area, as well as the site facilities provided by PETROAMAZONAS Company, we selected a number of paddocks used to cultivate pasture for livestock as control sites, and three types of sites within the petroleum extraction facilities (hereby referred to as “disturbed sites”), all of which differed in substrate compaction and contamination by hydrocarbons and heavy metals. The petroleum extraction process begins with the selection of a site, the removal of the vegetation and upper soil layer, and the creation of oil-platforms where oil drilling will occur. These drilling activities create contaminated residue material called “drilling mud” and “drill cuttings”, which are solids that are found in the drilling stream. These solids are then transported to an area called “mud and drill cutting

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Fig. 1. Location of the different plots within sites: the oil-platform (Platforms) plots are in blue; the mud and drill cutting cells (Cells) plots are in light green; the contaminated soil treatment units (CSTU) plots are in orange and the control, undisturbed site (Control) plots are in brown. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article).

cells”. Each cell contains a treatment pool where the drilling residue is mixed with chemical products to create a stabilized, homogenous mixture (Scholten et al., 2000; Kincannon, 1972). Additionally, other platforms called “contaminated soil treatment units” are built, where treatment is carried out on soils that have been contaminated by hydrocarbons as a result of crude oil spills that may occur for various reasons. Our disturbed sites were selected in above mentioned units within the oil field: 1) the oil-platform (hereby referred to as “Platform”) that corresponds to the margins that circumscribe the oil wells, where superficial soil layer and vegetation have been removed. This area has no contact with hydrocarbons or other residues (Fig. 2a); 2) the mud and drill cutting cells (hereby referred to as “Cells”; Fig. 2b), and; 3) the contaminated soil treatment units (hereby referred to as “CSTU”; Fig. 2c). In

all four sites, 20 plots (1600 m2 each one) were established (13 on Platforms, 3 in Cells, 2 in CSTUs, and 2 on Control sites). In each plot, we planted in rows six-month-old saplings – five specimens of each of the 20 selected species (100 specimens per plot). Each sapling was at least 4 × 4 m away from any other plant. Plants that died due to posttransplanting shock within the first month were replaced with new specimens of that same species. 2.2. Species selection We selected 20 tree species (15 native to the Amazon Basin and 5 exotic). The selection of these species was based on the following criteria: the native species must be ubiquitous in the Ecuadorian Amazon

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Fig. 2. Photos taken from: a) the oil-platform (Platforms); b) the mud and drill cutting cells (Cells); c) the contaminated soil treatment units (CSTU), and; d) undisturbed site (Control).

rainforests (Valencia et al., 1994); six of those selected were species dominant in early secondary succession stages. The mix of pioneer and non-pioneer species promotes long-term development and maintenance of forest structure (Ashton et al., 2001; Elliott et al., 2003). Due to the lack of silvicultural knowledge of native tree species, 5 exotic tree species were selected for their ability to grow rapidly on degraded lands (D'Antonio and Meyerson, 2002). All species (native and exotic) had wide geographic distributions, had seeds that were available in the surrounding forests all year round, had been used in reforestation

programs since 2000, and were of socio-economic importance for the local populations mainly due to their multiple uses (timber, ornamental and food, Villacís et al., 2016; Table 1). Seeds were collected from November 2010 to June 2011, and were subsequently transported to the nurseries. Each seed was planted in a germination tray filled with a substrate prepared in the nursery (black soil originating from riverbanks and coffee subproducts in a 1:1 volume proportion, a 10–30–10 N, P and K proportion, and lime). Once saplings reached a height of approximately 5 cm, they were placed in 1-L plastic

Table 1 Scientific name, family, use and typical succession stage of each forest species analyzed in this study. All species are native to the Ecuadorian Amazon except the last five, which are exotic (these originate from Asia, save for Leucaena leucocephala, which comes from Mexico). Scientific name

Family

Use

Ecological groups

Apeiba membranacea Spruce ex. Benth Cedrela odorata L. Cedrelinga cateniformis (Ducke) Ducke. Guarea purusana Inga densiflora Benth. Myrcia aff. Fallax Myroxylon balsamum (L.) Harms. Ormosia macrocalyx Piptadenia pteroclada Benth. Platymiscium pinnatum (Jack.) Dougand. Schizolobium parahyba (Vell.) S.F.·Blake Stryphnodendron porcatum D.A.Neill & Occhioni f. Tapirira guianensis Aubl. Vitex cymosa Bertero ex Spreng. Zigia longifolia (Humb & Bond. ex Willd.) britton & Rose Nephelium lappaceum L. Leucaena leucocephala(Lam.) de Wit. Flemingia macrophylla (Willd.) Merrill Syzygium jambos (L.) Alston Syzygium malaccense (L.) Merr. & L. M. Perry

Tiliaceae Meliaceae Fabaceae Meliaceae Fabaceae Myrtaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Anarcadiaceae Verbenaceae Fabaceae Sapindaceae Fabaceae Fabaceae Myrtaceae Myrtaceae

Ornamental Timber yield Timber yield Timber yield Fruit production Timber yield Timber yield Timber yield Timber yield Timber yield Timber yield Timber yield Timber yield Timber yield Timber yield Fruit production Fodder Fodder Fruit production Fruit production

P P P NP P NP P NP NP NP P NP NP NP NP – – – – –

P, pioneer species; NP, non-pioneer species.

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bags filled with the same substrate. They were then taken to the pre-acclimatization area (they were exposed to a mere 25% of the intensity of exterior light) for a period of two months, and finally to the acclimatization area under 100% sun exposure for two months before their transplanting. During the transplanting, the holes were dug with a dibber (60 × 60 cm); the soil extracted from the hole was thoroughly mixed with 5 kg of coffee subproducts, and was again placed in the hole with the plant. 2.3. Variables measured Sapling survival was measured two years after seedling transplanting; the bottle-neck period for plant establishment in tropical forests is usually between one to two years after planting (Holl et al., 2000; Hooper et al., 2002). Plant survival for each species was calculated by dividing the number of two-year-old living plants by the initial number of plants transplanted in each plot. Every four months over the course of the experiment we visually determined the cause of death of dead saplings. Causes of sapling mortality are usually diverse and unpredictable in many habitats (Fenner, 1987), but in some cases there are some clear signs that may point to a probable cause. In our study we classified the possible causes of sapling mortality into five classes according to the following signs: 1) death caused by competition with weeds (there was a dense cover of weeds around the base of the saplings; 2) death caused by drought (the substrate was dry compared to other treatments and dead plants only had the standing stem, which was completely dry); 3) death probably caused by excess of soil humidity and presence of hydrocarbons in the soil surface (plants were completely rotten and there were signs of hydrocarbons in the substrate); 4) insect attacks (plants had withered stems and leaves with insect holes) and, finally; 5) herbivory (clear signs of herbivory by mammals and/or other macrofauna). Additionally, every four months we carried out mechanical controls using weed whackers, eliminating all weeds within a 1 m radius of the saplings' stems. For each plot, we determined the diameter and height of each sapling at the time of transplanting (March 2012) and at the end of the experiment (March 2014). The diameter of trees was measured 10 cm from the base of the plant using a digital caliper with an error of ± 0.01 mm. The height of each plant was measured from the base to the apical meristem of the tallest stem, using a laser hypsometer (Impulse 200, US). We determined the relative growth rate in height (RGRheight) and diameter (RGRdiameter) in all surviving plants using the following equations: RGRheight (m/month) = [ln (final height) − ln (initial height)]/24 months; and RGRdiameter (cm/month) = [ln (final diameter) − ln (initial diameter)]/24 months (South, 1995). In order to compare species performance, we calculated the Integrated Response Index (IRI), which takes into account survival rates and growth variables, and serves to determine the performance of a sapling's species in an integrated manner: IRI = survival percentage × RGRheight × RGRdiameter (De Steven, 1991; Elliott et al., 2003). 2.3.1. Soil variables For each plot, we systematically collected 10 subsamples from the first 10 cm of soil in order to create a composite sample, both at the beginning (transplanting) and at the end of the experiment (two years afterwards). We analyzed the following properties: particle size distribution (relative content of sand, silt, and clay) using the hydrometer method; soil organic matter (SOM) content using dry combustion; the content of K+, Ca2 +, Na+, Mg2 +, Fe3 +, Cu2 +, Zn2 +, and Mn2 + using the Melich extractant and quantified with an atomic absorption spectrophotometer (SAVANT-AA Σ, USA); Al3 + and Al + H via the NaOH titration method; and, lastly, electrical conductivity (EC) and pH, both in soil suspension 1:10 (w:v) with conductivity- and pH-meters (Thermo Scientific, USA). All techniques are described in Sparks (1996). In Cells and CSTU sites, total petroleum hydrocarbons (TPH)

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and polycyclic aromatic hydrocarbons concentrations (PAH) with gas chromatography were estimated (SHIMATZU GC-2014, Japan). We also determined the concentration of cadmium (Cd), nickel (Ni), and lead (Pb) in soils using atomic absorption spectrometry (SHIMATZU AA-6800, Japan) and following the EPA SW-846 method (U.S. EPA, 1995). Limits of detection (LOD) for TPH, Cd, Ni, and Pb were calculated with the following equation: LOD = 3 × (sd/m); where “sd” is the standard deviation of 10 blank control samples and “m” is the slope of the calibration curve for each run. The quality assurance and quality control QC/QA protocols were performed using the standard addition method, and it was found that the recovery for TPH, TPHs, Cd, Ni, and Pb for atomic absorption spectrometry ranges from 94 to 105%. 2.4. Experimental design and data analysis Saplings from each forest species were planted in 20 plots that were then distributed in each of the four sites – or “treatments” – as follows: (i) 13 plots in Platforms; (ii) 3 in Cells; (iii) 2 in CSTUs; and (iv) 2 in Control sites (slope, soil type, and micro-environmental conditions were the same for all sites). Within each plot, we randomly designated 20 subplots, and planted five specimens of each of the 20 species within each subplot. For the comparison of treatments and species, a variance analysis was conducted using general linear mixed models. The initial height and diameter of each sapling were used as covariates. Only survival was transformed into arcsine; the rest of the variables were normally distributed. In order to analyze the cause of death, we used a generalized linear mixed model with a binomial distribution, where the variable was the number of plants that perished due to a particular cause and without distinction between species, and the offset was the total number of dead plants. Due to the presence of a significant interaction species × site in IRI responses, specific species recommendations had to be made for each site (i.e., types of soil). Based on IRI, we used the GGE (Genotype and Genotype by Environment interaction) biplot method (Yan and Kang, 2003) to determine which species exhibited the best performance in each site. This method is carried out by conducting an ANOVA for the integrated response index IRI, using a linear model that only contains the effect of the site; in this way, the residuals of this model include the effects of species and of site interaction × species. The residuals of the model are then placed in a new matrix where rows correspond to species and columns to sites. Using this data matrix, a principal component analysis (PCA) is conducted, with each site constituting a variable and each species constituting an observation. A graphic biplot is then created using the first two principal components (Gabriel, 1971); a polygon is drawn in the PCA space, formed by the extreme points of species, as are lines that start from the biplot origin and perpendicularly intersect each polygon side (Casanoves et al., 2005; Yan et al., 2007). Sites between two perpendicular lines are considered to be one particular environment, and those species that are farthest away from the center of the biplot and lie inside this environment are the species that performed best at that particular site and that can be recommended for reforestation at that site. Finally, differences in soil properties across the four sites were tested using variance analyses, assuming a completely randomized experiment design. Treatment means were compared using the LSD Fisher post-hoc test (p b 0.05). Analyses were conducted using glm and glmer functions in software package R v.3.2.3 (version 3.2.1.) using the implemented interface in InfoStat (Di Rienzo et al., 2015). 3. Results 3.1. Survival and growth Species differed in their plant survival rates at the end of the experiment (p b 0.0021). However, the type of soil substrate (treatment) did not have a significant effect on plant survival (p = 0.6849), nor did plant survival for each species differ across sites (there wasn't a significant

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Table 2 Plant mortality percentage (relative to each site) within each possible death category (cause of death) of saplings of 20 forest species after two years growing in three oil-field sites (Platforms: oil-platforms; Cells: mud and drill cuttings cells; CSTU: contaminated soil treatment units) and one undisturbed site (Control) in the Ecuadorian Amazon. Empty cells indicate that none of the dead plants seem to have died as a result of that category of cause of death. Values are means+/‐ SE. Different letters in the same row indicate significant differences (LSD Fisher post-hoc test, p b 0.05). The number after each site category denotes the number of plots per site. Cause of death

Platforms (n = 13)

Cells (n = 3)

CSTU (n = 2)

Control (n = 2)

Weeds Drought Humidity/surface hydrocarbons Insects Herbivory

59.15 ± 3.37 b 15.96 ± 2.51 a 24.88 ± 2.96 a

62.99 ± 4.28 b

3.77 ± 2.62c 16.98 ± 5.16 a 77.36 ± 5.75 a 1.89 ±1.87

96.15 ± 2.67 a 3.85 ± 2.67 a

14.17 ± 3.09 a 22.83 ± 3.72

statistical interaction species × site; p = 0.8167). Neither the potential effect of the covariates' diameter (p = 0.9981) nor the potential effect of the initial height (p = 0.8116) were significant. In any case, mean survival rate for all forest species was as high as 88.51%, and 17 (of 20) species exhibited an average survival rate over 80%. None had survival rates lower than 70% (Table S1). The presence of hydrocarbons in the contaminated substrates (Cells and CSTUs) did not affect plant survival as plants survived in these substrates at rates equal to those of plants in uncontaminated substrates (Platforms and Control). Saplings planted in CSTUs tended to have higher survival rates than those in the rest of the treatments. The comparative analysis of the possible natural causes of death revealed that the main cause of sapling death was weed interference (mainly Brachiaria brizantha and Pueraria phaseoloides); furthermore, there were differences between sites in the number of dead plants outcompeted by weeds (p b 0.0001). Humidity/surface hydrocarbons and drought also caused the death of plants in oil field substrates, although they did not exhibit any significant differences between sites (Table 2). Mean values for base diameter, height, RGRheight, and IRI differed among species within each site (specie × site interaction had a significant effect, Table 3). This was not the case with RGRdiameter, which differed between species (p b 0.0001) and, additionally, between sites (p = 0.0069). The covariate initial height significantly disturbed the response of all variables save for final height, suggesting that initial sapling height influenced plant performance during the following two years; however, the covariate initial diameter only significantly influenced RGRdiameter (Table 3). Plants in Platforms and Cells had the widest diameter. Conversely, individuals that grew in CSTUs and Control sites had much narrower diametric ranges (Fig. 3). As with the diameter, the greatest height range was observed in Platforms and Cells, while in CSTU and Control plots plant height values were lower (Fig. 4). Based on the Integrated Response Index (IRI, Table S2) the GGC analysis isolated which species had the best performance in terms of survival and growth in each of the sites studied (Fig. 5). The first two axes of the resulting PCA explained 83.7% of total variation. Plants from the species Flemingia macrophylla, Myrcia aff. fallax, Piptadenia pteroclada, Platymiscium pinnatum, and Zygia longifolia exhibited similar performances in oil field sites (Platforms, Cells and CSTU) and performed the best (excellent performance) compared to other species. At the other extreme lies a group of plants from the species Cedrelinga cateniformis,

Guarea castanea, Myroxylon balsamum, Nephelium lappaceum, and Vitex cymosa, which exhibited poor performances in the oil-field sites. In the control sites, Apeiba membranacea, F. macrophylla, Leucaena leucocephala, M. aff. Fallax, and Z. longifolia exhibited excellent performance levels, whereas C. cateniformis, G. castanea, Ormosia macrocalyx, P. pinnatum, and Stryphnodendron porcatum performed poorly. The remaining species exhibited average performance levels irrespective of which site they were planted in. (Table 4) 3.2. Soil characteristics At the beginning of the experiment, there were significant differences in pH, Fe3 +, Mn2 +, Al3 +, Ca:Mg ratio, and SOM values among soil substrate types (Table 5). Undisturbed soil (Control) exhibited higher pH and SOM values than other substrates. Soil substrate in Cells exhibited higher concentrations of Mn2 +. Soil substrates from Platforms and Control sites exhibited the highest values of Fe3+, whereas soil substrates from CSTU sites exhibited higher concentrations of Ca2+, K+, Na+, and CE, as well as higher values of Al3+, Ca:Mg ratio, and Al + H content. Additionally, significant differences were found in TPH values between CSTU and Cells sites (Table 5). At the end of the experiment and compared to the initial conditions, Platforms exhibited significant increases in pH, SOM, Fe3 +, Zn2 +, and cation ratio ((Ca + Mg) / K) values, which were associated with an increase in Mg2 +; similar tendencies were found in the remaining three sites, where there were only significant increases in Mg2+ contents and significant decreases in exchangeable sodium in the substrate of CSTU (Table 5). Moreover, soils of Cells and CSTUs exhibited significant decreases in TPH contents compared to pre-planting conditions, with, circa 11 to 22% decreases in TPH levels, respectively. 4. Discussion This study provides a preliminary list of the most suitable species for the reforestation of areas disturbed by petroleum extractions in the Ecuadorian Amazon. Even though there are numerous extant studies of forest species performance in the tropics (Shono et al., 2007; Wishnie et al., 2007), this is the first research on forest species performance in soils disturbed by petroleum extraction in the Amazon Basin. At the beginning of the experiment, soil characteristics in the disturbed sites were unfavorable to vegetation growth due to poor aeration, elevated acidity, low chemical fertility, imbalance of bases and, in two substrates,

Table 3 Results from the covariance analysis for different plant growth variables 24 months after transplanting. df is degrees of freedom, F is the resulting F-Fisher value, and P is the resulting probability. Species (20 species) and site (3 disturbed and one control) were considered fixed factors, whereas plant initial diameter and height were considered covariate variables. Source

Species Site Initial diameter Initial height Species × Site

df

19 3 1 1 57

Diameter

RGR diameter

RGR height

F

P

F

Height P

F

P

F

P

F

IRI P

6.87 7.66 1.04 3.97 1.77

b0.0001 0.0021 0.3084 0.0474 0.0014

7.98 9.51 1.08 1.67 2.18

b0.0001 0.0008 0.2996 0.1980 b0.0001

5.70 5.82 77.89 10.41 1.21

b0.0001 0.0069 b0.0001 0.0014 0.1620

7.58 8.54 0.60 149.44 1.95

b0.0001 0.0013 0.4408 b0.0001 0.0002

9.25 3.93 3.44 53.15 3.44

b0.0001 0.0281 0.0648 b0.0001 b0.0001

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contamination by hydrocarbons and heavy metals. However, after two years of growth in the contaminated sites, most species exhibited survival rates of over 80% and overall improved soil conditions and decreased hydrocarbon levels in soil substrates. Based on the integrated growth index, 5 of the 20 forest species exhibited excellent performance levels and, therefore, are the most suitable for use in restoration projects. 4.1. Soil characteristics Soils from disturbed sites exhibited SOM contents between 0.3% and 0.6%, as all vegetation and the entire superficial soil layer (approximately 20 cm deep) had been previously eliminated; undisturbed sites colonized by pastures exhibited 4 to 8 times more SOM. Increases in SOM, Fe, Zn, and Mn in the disturbed sites suggest that soil redox conditions improved towards the end of the study. Overall, increased organic compounds in soil substrates from Cells and CSTUs may alleviate the amount of soil contamination due to hydrocarbons, as was found by Helmy et al. (2015), who added glucose in such contaminated soils and recorded increased activity in oil-degrading bacteria. An increase of 0.3 to 0.9 pH units in all disturbed sites two years after planting could be considered another indicator of the beneficial effect of planted trees on these soils. One of the characteristic traits of soils that are as rich in oxidants as those of the Amazon is their amphoteric behavior (Besoain, 1985), which considerably increases the buffering capacity of the soil, rendering it difficult to elevate pH under these conditions. We also found significant decreases in exchangeable sodium in the substrate of CSTU compared to initial conditions. However, Exchangeable sodium percentage in all sites and periods was quite low (range 0.8 to 4.7%) and therefore it probably would not have interfered in saplings yield (Tewari and Singh, 1991). Overall, previous studies have highlighted the important role played by soil characteristics on the speed at which the soil is degraded when hydrocarbons are present (Alrumman et al., 2015). Soil properties control the effect of contaminants on the diversity and functionality of microbe communities, which are particularly affected by soil pH (Bardgett and Wardle, 2010). One of the distinctive characteristics of petroleum-contaminated soils is their poor aeration, which affects microbe processes and soil microelement contents. For this reason, bioremediation techniques usually begin by trying to improve aeration; plant roots play a key role in accelerating such soil aeration improvement (Mohsenzadeh et al., 2010), which may have also occurred at the sites surveyed by this study following two years of vegetation growth. The concentrations of TPH in Cells and CSTU sites were higher than permissible at the beginning and end of the experiment (MAE, 2001). However, the concentration of TPH decreased at the end

Fig. 3. Basal stem diameter of saplings of 20 forest species after two years of growth in three sites disturbed by petroleum extractions (Platforms: petroleum platforms; Cells: mud and drill cuttings; CSTU: contaminated soil treatment units) and in one undisturbed site (Control) in the Ecuadorian Amazon. Symbols and bars are mean values ± SE.

Fig. 4. Plant height of saplings of 20 forest species after two years of growth in three sites disturbed by petroleum extractions (Platforms: petroleum platforms; Cells: mud and drill cuttings; CSTU: contaminated soil treatment units) and in one undisturbed site (Control) in the Ecuadorian Amazon. Symbols and bars are mean values ± SE.

of our experiment, demonstrating that the studied species can reduce hydrocarbons levels in contaminated soils. This is in accordance with Karamalidis et al. (2010) who found that soil aeration induced by root growth and increased nutrient levels via litter deposition and organic matter accretion may drastically reduce hydrocarbons in contaminated soils. 4.2. Species performance The highest survival rates among species occurred in the contaminated soil treatment units (CSTU); note that CSTUs had the greatest hydrocarbon concentrations across sites. However, plants exhibited lower growth rates here than in any other site. This is in accordance with results in Merkl et al. (2005) and Shirdam et al. (2008); these authors also found impaired growth in plants that grew on petroleum contaminated soils in tropical coastal areas. Excess humidity in the presence of hydrocarbons seemed to be the main cause of death in the CSTUs; this humidity was probably due to not only the clay-like texture of the soil, but also to the surface migration of hydrocarbons, which may have caused leaf necrosis, a reduction in photosynthesis, and a reduction of aboveground and belowground biomass in plants from our experiment, as reported in other extraction sites (Adam and Duncan, 2002). Our results and those from Quiñones-Aguilar et al. (2003) show that species tolerance to hydrocarbons varies from one species to another; therefore, tree species that have the capacity to grow well in the CSTUs – such as F. macrophylla, Myrcia aff. fallax, P. pteroclada, P. pinnatum, and Z. longifolia – should be used in remediation programs

Fig. 5. GGE biplot that shows which species showed the best performance in each site (Platforms: petroleum platforms; Cells: mud and drill cuttings; CSTU: contaminated soil treatment units; Control: undisturbed soil).

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well adapted to soils that are acidic, clay-like, and with low fertility levels (Vigna et al., 2011) such as those from our sites, and they compete fiercely with trees (Casselman et al., 2006), preventing the natural regeneration of native forest species (Holl et al., 2000). This suggests a need to conduct more frequent mechanical controls on weeds, at least during the first year after planting (Craven et al., 2009). However, these weeds may have had some positive effects on disturbed soils prior to reforestation. Studies conducted in the Venezuelan savannah indicate that multiple species of the genus Brachiaria effectively remediate petroleum-contaminated soils (Merkl et al., 2005). Another study conducted in France suggests that herbaceous legume species are most suitable for the rehabilitation of hydrocarbon-contaminated soils, due to the fact that they increase the amount of soil nitrogen and aeration (Gudin and Syratt, 1975). For this reason, the presence of these weed species prior to tree planting in our studied sites could reduce the amount of hydrocarbons in the soil and improve later tree growth if these weeds were eradicated just before tree planting. Plants of five species – F. macrophylla, M. aff. fallax, P. pteclorada, P. pinnatum, and Z. longifolia – exhibited excellent performance during the first two years in at least one of the oil-field sites studied. Of these species, all but one are native, and their ecological benefits would justify their use in rehabilitation programs. For example, F. macrophylla, P. pteroclada, P. pinnatum, and Z. longifolia – all leguminous species – exhibit dense root systems that protect soil from erosion, are nitrogen fixers, tolerate compaction and low fertility levels, and have considerable potential to remediate soil contaminated by petroleum because they facilitate oil-degrading bacterial communities (Bento et al., 2012). On the other hand, eight species – Cedrela odorata, C. catenaeformis, G. castanea, M. balsamun, N. lappaceum, O. macrocalyx, S. porcatum, and V. cymosa – were classified as poor for at least one of the sites and thus we advise against their use in restoration programs in these regions, as it is improbable that they would achieve the desired performance. Plants of the remaining species (Inga densiflora, Leucaena leucocephala, Schizolobium parahyba, S. porcatum, Syzygium jambos, Syzygium malaccense and Tapirira guianensis) – which exhibited average

Table 4 Qualitative classification of sapling performance for each species analyzed in three sites disturbed by petroleum extractions and one undisturbed site (see legend in Table 2) in the Ecuadorian Amazon. Classification was based on the integrated response index (Table S2). Letters E, R, and M represent the classification category according to species performance (E: excellent; A: average; P: poor). Species

Platforms

Cells

CSTU

Control

Apeiba membranacea Cedrela odorata Cedrelinga cateniformis Flemingia macrophylla Guarea purusana Inga densiflora Leucaena leucocephala Myrcia aff. Fallax Myroxylon balsamum Nephelium lappaceum Ormosia macrocalyx Piptadenia pteroclada Platymiscium pinnatum Schizolobium parahyba Stryphnodendron porcatum Syzygium jambos Syzygium malaccense Tapirira guianensis Vitex cymosa Zygia longifolia

A A P E P A A E P P A E E A A A A A P E

A A P E P A A E P P A E E A A A A A P E

A A P E P A A E P P A E E A A A A A P E

E A P E P A E E A A P A P A P A A A A E

to not only to restore vegetation cover but also to degrade and transform contaminating residues into less toxic compounds (Pilon-Smits, 2005). Plant survival rates in Platforms and Cells tended to be lower than in CSTUs and Control sites, but plant growth was disturbed less widely in the former. The main cause of death for species in our study seemed to be weed interference; our mechanical control every four months did not effectively eliminate two of the main weed species: the grass B. brizantha in the case of Control site (paddocks), and the leguminous vine P. phaseoloides in the case of Platforms and Cells. These weeds are

Table 5 Soil characteristics at the beginning and end of the experiment in three sites disturbed by petroleum extractions and one undisturbed site in the Ecuadorian Amazon (see legends in Table 2). Values represent the mean for each variable and site. Different lowercase letters indicate significant differences among sites within the phase of the study (beginning or end). Different capitalized letters in each site at the end of the experiment indicate differences between the values of the variable at the beginning and the end (two years after planting) of the experiment. The number after each site category denotes the number of plots per site.

Sand (%) Silt (%) Clay (%) SOM (%) pH Zn (mg kg−1) Cu (mg kg−1) Fe (mg kg−1) Mn (mg kg−1) Al (mg kg−1) Exchangeable Na (%) C.E. (dS m−1) Ca/Mg Mg/K (Ca + Mg)/K Al + H Total petroleum hydrocarbons (mg kg−1) (LOD =

Beginning

End

Site

Site

Platforms (n =

Cells (n =

CSTU (n =

Control (n = Platforms (n =

Cells (n =

CSTU (n =

Control (n =

13)

3)

2)

2)

13)

3)

2)

2)

20 37 43 0.6 a A 4.7 a A 1.8 A 3.8 45 ab A 24 ab 3.1 a 1.81 a 0.07 3.4 a 14.0 61 A 8.6 a

11 11 25 35 59 26 54 30 48.5 0.3 a 0.4 a 2.45 b 4.5 a 4.7 a 5.8 b 1.5 0.9 0.7 A 2.2 1.9 3.7 26 a 20 a 77 ab 47 b 7.7 a 2.9 a 2.7 a 10.3 b Sd 0.88 a 4.70 b A 1.36 a 0.06 9.3 0.07 3.6 a 16.9 b 7.6 ab 12.9 0.6 8.3 58.6 11.4 71.7 8.1 a 23.3 b 0.7 a 4685.60 a A 5997.86 b A

23 37 40 1.3 B 5.8 B 3.3 B 5 105 B 20.2 2.6 a 1.58 0.29 4.3 25.0 131.7 B 4.7 a

12 12 25 34 59 26 54 29 48.5 0.7 0.35 2.8 5.5 5.1 5.5 3.1 3.8 3.2 B 1.9 2.4 2.2 103 144 298 37.2 17.0 22.8 2.3 a 10.4 b 0.3 a 1.29 1.20 B 1.94 Sd Sd 0.04 4.5 3.4 7.8 26.7 36.7 16.3 146.7 160.0 143.8 5.8 a 24.8 b 1.1 a 3621.01 a B 5304.04 b B

32 mg kg−1) Polycyclic aromatic Hydrocarbons (mg kg−1) (0.3

b0.3

b0.3

mg kg−1) Cd (mg kg−1) (LOD = 0.2 mg kg−1) Ni (mg kg−1) (LOD = 5 mg kg−1 Pb (mg kg−1) LOD = 5 mg kg−1)

1.28 32.11 23.79

1.83 34.29 23.73

b0.3 1.21 30.49 23.15

1.67 33.97 23.54

b0.3

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performance in all sites – could be categorized as species with a moderate potential for the reforestation of areas disturbed by petroleum extractions in the Ecuadorian Amazon. However, they would require permanent care if they were to reach their maximum growth, and their selection ought to be based on the ecological benefits they may produce. This would also be an investment in better soil water management, as forests restored in similar degraded lands (such as mines) will contribute to the reduction of runoff and to the improvement of soil quality (Mukhopadhyay and Maiti, 2014; Buendia et al., 2016; Jiménez et al., 2016; Rivas-Pérez et al., 2016), reducing the off-site detrimental effects these mining and oil extraction activities may have (e.g., export of contaminated sediments and polluted water). 5. Conclusion Just two years after the reforestation of different sites in oil fields in the Ecuadorian Amazon that differed in soil substrate contamination, we documented an improvement in soil substrate characteristics. There was a substantial decrease in hydrocarbon levels (up to 22% from initial conditions) in contaminated substrates from the mud and drill cutting cells and the contaminated soil treatment units. Uncontaminated but compacted soil substrates from oil-platforms showed an overall improvement in their physicochemical characteristics. Plants from the species F. macrophylla, M. aff. fallax, P. pteroclada, P. pinnatum, and Z. longifolia exhibited the best survival and growth across sites and would be the most suitable species to be used for the potential rehabilitation of oil-field sites in Ecuadorian Amazon. These species may be useful in the restoration of areas disturbed by oil extractions in the tropical forests of the Amazon Basin, as the same oil extraction process is conducted throughout the region using similar technologies, all but one of these species are native, and the species studied have a wide geographical distribution throughout the Amazon Basin. Acknowledgements We thank SENESCYT for their financial support (SENESCYT-DMPF2012-0470-MI) and Tauro Corporation for their field work support. Sites for the trial were provided by EP PETROAMAZONAS, for which we are grateful. We are grateful to Rocio C. Labrador for her language revision. CA received a “Ramón y Cajal” research contract (RYC-201212277) from the Spanish Government. Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2016.05.102. References Adam, G., Duncan, H., 2002. Influence of diesel fuel on seed germination. Environ. Pollut. 120, 363–370. http://dx.doi.org/10.1016/S0269-7491(02)00119-7. Alrumman, S.A., Standing, D.B., Paton, G.I., 2015. Effects of hydrocarbon contamination on soil microbial community and enzyme activity. J. King Saud Univ.-Sci. 27, 3–41. http://dx.doi.org/10.1016/j.jksus.2014.10.001. Ashton, P.M.S., Gunatilleke, C.V.S., Singhakumara, B.M.P., Gunatilleke, I.A.U.N., 2001. Restoration pathways for rain forest in southwest Sri Lanka: a review of concepts and models. For. Ecol. Manag. 154, 409–430. Bardgett, R.D., Wardle, D.A., 2010. Aboveground-belowground linkages. Biotic Interactions, Ecosystem Processes, and Global Change. Oxford University Press, Oxford, UK. Bento, R., Saggin-Júnior, P., Rosa, O., Rosangela, R., Silva, E., Tavares, S., Landa, F., Martins, L., Volpon, A., 2012. Selection of leguminous trees associated with symbiont microorganisms for phytoremediation of petroleum contaminated soil. Water Air Soil Pollut. 223 (9), 56–59. http://dx.doi.org/10.1007/s11270-012-1305-3. Berendse, F., van Ruijven, J., Jongejans, E., Keesstra, S.D., 2015. Loss of plant species diversity reduces soil erosion resistance of embankments that are crucial for the safety of human societies in low-lying areas. Ecosystems 18, 881–888. http://dx.doi.org/10. 1007/s10021-015-9869-6. Besoain, E., 1985. Mineralogía de arcillas de suelos. IICA, Costa Rica (1205 pp). Bradshaw, A.D., Huttl, R.F., 2001. Future minesite restoration involves a broader approach. Ecol. Eng. 17, 87–90.

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