1. Introduction
Cultivated coffee is considered the world's leading agricultural commodity, with a market generating more than 90 billion dollars annually. Around 8% of the world's population (approximately 500 million people) are involved in the coffee market, from sowing to final consumption. Coffee is produced in 14 states of Mexico, of which Chiapas, Veracruz, Puebla, and Oaxaca account for 90% of production. In 2019, Chiapas contributed 40.9% of the national production, followed by Veracruz with 24.2%, Puebla with 16.0%, and Guerrero with 9.4% [
1]. The state of Veracruz is the second most important coffee-producing region in Mexico. The coffee is produced in 842 communities of 82 municipalities. Sixty percent of the coffee is grown above 750 m asl in elevation. The regions with the highest production are Coatepec, Cordoba, Huatusco, Misantla, and Atzalan. Currently, 21,089 producers in the central region of Veracruz produce this crop over a total area of 58,712 ha, representing 7.3% of the area dedicated to coffee growing nationally. The rural development district of Coatepec cultivates 28,873 hectares in 21 municipalities. Jilotepec belongs to this district and has a planted area of 1,776 hectares [
2].
Coffee growing is considered a fundamental strategic activity, because it allows the integration of productive chains, as well as the generation of foreign currency and employment, and is the means of subsistence for many small producers and indigenous groups [
3,
4]. In addition, it is of great ecological importance since more than 90% of the area cultivated with this crop is under shade, which contributes to biodiversity conservation and provides vital environmental services to society [
5,
6]. In Mexico, the soils where coffee is produced are generally of volcanic origin and are characterized by an acidic pH of 4.5-5.2, as well as low availability of essential macronutrients such as phosphorus (P) [
7]. This is mainly because this element is associated with other ionic elements such as calcium, iron, and aluminum, present in forms that cannot be assimilated by the plants [
8]. The amount of available P depends on the modification of the dynamic equilibrium that maintains the dissolution of insoluble inorganic compounds and on the decomposition of organic matter [
9]. Phosphorus is important in coffee cultivation since it plays key roles in many plant processes such as energy metabolism, the synthesis of nucleic acids and membranes, photosynthesis, respiration, nitrogen fixation, and enzyme regulation [
10]. During the early stages of coffee plant development, this element is responsible for vigorous plant growth, participates in the formation of effective root systems, and acts as a promoter of flowering and fruit development. During the reproductive stage, phosphorus is essential for the formation, growth, and multiplication mechanisms of the flower organs. Phosphorus deficiency in the soil can be observed in coffee plants through the yellowing of leaves and a lack of fruit ripening. In severe cases, the leaves near the ripening fruit fall off completely. To remedy a lack of P, coffee producers apply large amounts of phosphate fertilizers [
1], although 75-90% of the phosphate added precipitates through the formation of metal cation complexes [
11]. In addition, excessive use of fertilizers leads to eutrophication, water toxicity, groundwater contamination, air pollution, soil and ecosystem degradation, biological imbalances, and reduced biodiversity, so it is necessary to seek another option to release P from inorganic and organic pools of total soil P. One alternative is the application of bioinoculants, which are preparations of microorganisms for inoculation with the aim of partially or completely replacing inorganic fertilization.
In this context, phosphate solubilizing fungi (PSF) are of great importance since they are a functional group of microorganisms that play a fundamental role in the P cycle. Thanks to the activity of these fungi, plants can take advantage of the large reserves of insoluble phosphorus fixed to soil minerals [
12]. Some fungi and bacteria can solubilize P from unavailable forms in the rhizosphere. The mechanism of mineral phosphate solubilization by the strains of PSF is associated with the release of low molecular weight organic acids [
13], which, through their hydroxyl and carboxyl groups, act to chelate the cations bound to the phosphate, thereby converting it into soluble forms. Phosphate solubilizing fungi can produce extracellular enzymes, i.e. a group of phosphatase enzymes that can mineralize organic P into inorganic P such that the P becomes available for the plants. There are several soil phosphatases, the most common of which are phosphomonoesterases, phosphodiesterases, and phytases. Phosphomonoesterases act on phosphate monoesters and, according to their optimum pH, are categorized into acid and alkaline phosphomonoesterases. These microorganisms have a high potential for promoting plant growth by increasing soil fertility [
14]. In agricultural soils, the use of microbial inoculants (biofertilizers) that present P-solubilizing activities is considered an environmentally friendly alternative to further applications of chemical-based P fertilizers [
11]. The coffee rhizosphere is associated with many beneficial organisms, including growth-promoting microorganisms that may contribute to fulfilling the nutritional requirements of the plant. The objective of this study was to evaluate the PSF and to obtain further information about the mechanisms involved in the solubilization of P, as well as to evaluate the effect of inoculation of an PSF strain on coffee plants under field conditions.
3. Discussion
For this study, a high percentage of the total number of strains evaluated formed solubilization halos (79.4%). This result is higher than the percentage detected by Posada et al., [
16], who report only 9.73% of the strains isolated from coffee plantations in Mexico, and slightly higher than that reported by Arias et al., [
17] (71.5%) from the rhizosphere of coffee plants in Mexico (
Coffea arabica var. Costa Rica). The results of this study confirm that shaded coffee plantations and tropical montane cloud forest harbor a high number of soil fungi with phosphate solubilizing capacity. Due to the presence of different tree species native to the cloud forest and the high diversity of plant species in the shaded coffee plantations, these sites have a considerable accumulation of plant debris that, once decomposed, increase the humus content of the upper soil horizons. This could explain the high number of solubilizing species, given that the presence of a high population of solubilizing micromycetes has been positively related to soil organic matter content [
18]. Another contributing factor could be the metabolic activity of the plant roots through exudates [
19]. The high population of PSF could also be related to the presence of certain nutrients, pH, moisture content, organic matter, and some soil enzyme activities [
20]. Djuuna et. al., [
21] detected a correlation between the number of PSF and the level of soil P availability and moisture content, indicating an increase in soil P availability with a greater abundance of PSF in the soil. Some strains of filamentous fungi have been studied in research involving species of the genera
Alternaria [
22,
23],
Aspergillus [
24],
Eupenicillium [
25],
Fusarium [
26],
Cladosporium [
27],
Gongronella [
28]
Helminthosporium [
29],
Mortierella [
30]
Rhizopus [
22],
Talaromyces [
28,
31],
Trichoderma [
32], prominent among which are the
Aspergillus y
Penicillium [
32,
33].
In this study, the following 21 genera presented a positive response to the solubilization of Ca
3(PO
4)
2:
Anungitopsis, Arthrographis, Aspergillus, Beauveria, Gliocephalotrichum, Nigrospora, Chrysosporium, Cordana, Cylindrocarpon, Eladia, Geomyces, Merimbla, Nectria, Oidiodendron, Penicillium, Phialomyces, Phialophora, Pseudogliomastix, Sagenomella, Sporotrix, and
Umbelopsis. Several studies indicate that the genera
Aspergillus and
Penicillium have a high capacity for solubilization of phosphates of Ca, Al, and Fe [
34,
35,
36,
37,
38,
39].
The results obtained here corroborate the high phosphate solubilizing capacity of the
Penicillium and
Aspergillus species. Of the 25
Penicillium species evaluated, 23 formed solubilization halos, and all strains corresponding to the genera
Eupenicillium and
Talaromyces, which are sexual or perfect stages of
Penicillium, were positive. Species of the
Penicillium genus are the most studied as phosphate solubilizers, and have produced the strains that are currently used as biofertilizers; e.g., the product Fosfosol© marketed in Colombia [
40,
41] and mainly aimed at rice cultivation, with the active ingredient
Penicillium janthinellum. In Canada, JumpStart®, produced from a strain of
Penicillium bilaiae and tested on wheat, has been marketed since 1990. As with
Penicillium, most of the
Aspergillus strains tested had positive responses to solubilization. In this case, five of the six strains formed halos, with four of these reaching scale III.
In this study, the range of solubilization rates (RSR) was 3.5 to 3.8. These values are higher than those reported by Morales et al. [
42], who report a maximum RSR of 1.3 for strains of
Penicillium albidum, P. thomii, P. restrictum, P. frequentans, Gliocladium roseum, and
Penicillium sp. Elías et al. [
43] report an RSR of 2.87 for
Aspergillus sp., Hernandez et al. [
44] report an RSR of 3 for
Paecilomyces lilacinus, and Verma and Ekka [
45] report 2.25 for
Penicillium purpureogenum. Other studies have reported phosphate solubilization rate values of up to 5.3 RSR for
Trichosporon beigelii [
46]. Romero-Fernandez et al. [
47] report ranges of 2.06-6.85, the latter value for a
Penicillium strain. In a study of strains isolated from the rhizosphere of
Coffea arabica var. Costa Rica, Arias et al. [
17] present RSR values in a range of 1.13-6.5. The use of revealing tests using halos in solid culture media and RSR data is a tool with which to detect the phosphate solubilizing capacity of strains rapidly and easily; however, the formation of halos in solid media should not be considered the only test for evaluating solubilization capacities. Quantitative tests are also necessary since Arias et al. [
17] did not find a significant relationship between RSR in a solid medium and solubilized phosphorus content in a liquid medium.
In the quantitative evaluation, the absence of soluble P in the controls clearly demonstrates that all three strains tested are phosphate solubilizers and that the manipulation of the cultures was appropriate. The
A. niger strains solubilized a high amount of insoluble phosphorus at 98.22 mg/L, followed by
P. waksmanii at 95.77 mg/L and
P. brevicompactum at 74.63 mg/L. The values presented here exceed those highlighted in other studies [
17,
37,
42,
44,
48,
49,
50,
51]. However, they were lower than the values presented for the
Aspergillus sp. strain (167.7 mg/L) [
37].
Several authors argue that fungal species use the production of organic acids as a solubilization mechanism, reflected in a reduced pH [
52,
53,
54]. The data presented here showed that Ca
3(PO
4)
2 can be solubilized by lowering the pH of 1.9 The PSF have been shown to play a crucial role in phosphorus solubilization due to the production of organic acids.
Aspergillus niger and some
Penicillium sp. have been reported for solubilization of rock phosphate, phosphate mobilization [
35,
55]. Acidification of the growth medium through the production of organic acids can be explained by the utilization of glucose as a carbon source during growth. Similar results were extrapolated from previous studies [
56]. Organic acids secreted by fungi dissolve mineral phosphate because of the anion exchange of PO
43- for the acid anion [
57].
Seven different organic acids (salicylic, ascorbic, citric, formic, lactic, oxalic, and malic acid) were detected during in vitro phosphate solubilization. Solubilization by acidification depends on the nature and strength of the acid produced by the fungus since there are those such as tri- or di-carboxylic acids that are more efficient solubilizers than mono-basic and aromatic acids [
44,
58,
59]. Salicylic acid was the organic acid most produced by all the PSF. Its concentration was 1823.8 mg/l as produced by
Aspergillus japonicus. Salicylic acid was the most quantitatively produced organic acid for all PSF isolates which has an important role in defense mechanisms against biotic and a biotic stress [
54].
Some research has reported that enzymes, such as acid phosphatase and phytases, are involved in P solubilization [
58,
60,
61,
62,
63]. These enzymes cleave the ester bond of the insoluble forms of P, leaving orthophosphate ions that can be assimilated by plants [
64]. Previous reports indicate that the genera
Aspergillus and
Penicillium both actively participate in the mineralization of soil organic P through the production of phosphatase enzymes [
65].
The results presented here evidence the production of acid phosphatase by the solubilizing fungi of the two strains of the genus
Penicillium and the strain of
A. niger. The highest production of acid phosphatases was detected in the
P. brevicompactum strain. These results support those obtained by Gomez [
66], who found that some
Penicillium species may have a higher capacity to produce acid phosphatases than
Aspergillus species. Similar reports were obtained by Valenzuela et al. [
67] who evaluated 180 fungal strains and found that
Penicillium strains showed a higher activity of this enzyme than was produced by
Aspergillus strains.
This study shows that the
A. niger strain was superior to the other strains in terms of its ability to solubilize tricalcium phosphate. Other studies report that
A. niger produces oxalic acid [
68] which could explain its higher P solubilization capacity compared to the other microorganisms. Solubilization in the
P. brevicompactum strain may be mostly achieved through the production of phosphatase enzymes since the results show that this strain presented the highest content of these.
Microorganisms harbored in the rhizosphere of plants play several key roles in improving plant productivity, nutrient cycling, and soil fertility. Overall, in this field study conducted on three coffee plantations in Jilotepec, Veracruz, inoculation with the phosphate solubilizing fungus strain
P. brevicompactum increased productivity in the coffee plants. The phosphate solubilizing potential of the
P. brevicompactum strain had already been assessed on coffee (
Coffea arabica var. Garnica) plants by Perea et al. [
69]; however, that study was conducted under controlled conditions. In this study, the inoculation of PSF (both alone and together with mycorrhizae) favored the development and availability of phosphorus in the soil, as well as foliar phosphorus content. However, given that the study was carried out under controlled conditions and with 8-month-old seedlings, it was not possible to determine the effect of PSF on coffee bean production.
About the soil soluble phosphorus, this parameter increased after two months of inoculation with P. brevicompactum. In the second sampling (fourth month of inoculation), however, it had significantly reduced although the values remained higher in the plants inoculated with P. brevicompactum.
In the first sampling, the foliar phosphorus content increased but, by the second sampling, it had reduced significantly. Contrary to the results for soluble soil phosphorus, foliar phosphorus content was higher in the uninoculated plants. The subsequent decrease in both soil and leaf phosphorus content may have been because the solubilized phosphorus was being used by the plant in coffee cherry production. In a study in North Bengal in India, Chakraborty et al. [
70] evaluated the ability of some phosphate-solubilizing fungi to promote plant growth in soybean seedlings and found a reduction of phosphorus in the soil. In that study, the concentration of phosphorus was significantly increased in the roots. It is therefore recommended that further research be conducted to monitor the phosphorus in the plant from the roots to the leaves.
Several studies have documented the successful use of bioinoculants and they have been used as an alternative to traditional fertilization. In a study in Australia [
39] used bioinoculants based on
Penicillium bilaiae and
Penicillium radicum and showed beneficial effects on wheat crops. In Canada, a biofertilizer based on the fungus
Penicillium bilaiae was registered in 1990 for use on wheat and tested initially on a few hectares with good results and, in 2002, approximately one million hectares sown with principal crops in Canada were using this biofertilizer [
71].
In Colombia, a biofertilizer with phosphate-solubilizing microorganisms, the active ingredient of which is
Penicillium janthinellum, has also been marketed. This product was used in rice cultivation, producing high increases in the production of this cereal [
41]. The results obtained in this study are promising for the development of a bioinoculant of the fungal strain
P. brevicompactum; however, further research is required to establish appropriate doses and re-inoculation schedules. The vigorous microbial activities in soil optimize nutrient cycling and maximize the efficiency of their use in agronomy [
72]. A recent extensive review [
73] of greenhouse and field trials has shown a marked improvement in the growth responses of various crops to inoculations of phosphate-solubilizing microorganisms.
Most studies have been conducted with bacteria; however, although they are the main decomposers of organic matter and dictate soil carbon and other elements, the role of fungi is the subject of relatively little study. Many fungi can solubilize insoluble phosphates or facilitate P acquisition by plants and therefore form an important part of commercial microbial products, with
Aspergillus, Penicillium, and
Trichoderma being the most efficient [
74].
The use of bioinoculants, together with the rationalized use of phosphate fertilizers, is important and it is necessary to adjust fertilization levels (especially of P and N) to reduce the negative impact on the environment. Chemical-based agriculture has had a negative impact on beneficial microbial communities, significantly reducing microbial biodiversity. There is therefore a need to adopt ecological farming practices for sustainable agriculture. Indigenous or native microorganisms are considered an important tool with which to overcome problems associated with the overuse of chemical fertilizers and pesticides.
Although research has been conducted using phosphate-solubilizing bacteria and fungi in vitro on plant growth promotion, particularly in coffee (Coffea arabica L), there are few reports regarding their impact on growth under field conditions. This study is the first worldwide to evaluate the potential of this group of microorganisms on coffee bean production.
Figure 1.
Fungi showing phosphate solubilization leading to formation of clear zone in Sundara´s medium A: Aspergillus candidus; B: Aspergillus sclerotiorum; C) Acremonium roseolu;, D) Aspergillus sp. 1Y; E) Cladosporium cladosporioides; F) Eupenicillium euglaucum; G) Penicillium glabrum, H) Eupenicillium ludwigii, I) Fusarium sp. 25, J) Penicillium arenicola, K) P. glabrum; L) Penicillium waksmanii; M) Sagenomella diversispora; M) Paecilomyces marquandii; N) Aspergillus niger, O) Beauveria bassiana, P) Penicillium brevicompactum.
Figure 1.
Fungi showing phosphate solubilization leading to formation of clear zone in Sundara´s medium A: Aspergillus candidus; B: Aspergillus sclerotiorum; C) Acremonium roseolu;, D) Aspergillus sp. 1Y; E) Cladosporium cladosporioides; F) Eupenicillium euglaucum; G) Penicillium glabrum, H) Eupenicillium ludwigii, I) Fusarium sp. 25, J) Penicillium arenicola, K) P. glabrum; L) Penicillium waksmanii; M) Sagenomella diversispora; M) Paecilomyces marquandii; N) Aspergillus niger, O) Beauveria bassiana, P) Penicillium brevicompactum.
Figure 2.
Figure 2. Soluble phosphorus and pH from extracts of three PSF strains (A. niger AN, P. brevicompactum PB, P. waksamnii PW) and the control (C), over 21 days of incubation (measured at 9, 12, 15, 18 and 21 days). Data are the average of three replicates ± standard error. Identical letters in columns indicate no significant difference (p≤0.05).
Figure 2.
Figure 2. Soluble phosphorus and pH from extracts of three PSF strains (A. niger AN, P. brevicompactum PB, P. waksamnii PW) and the control (C), over 21 days of incubation (measured at 9, 12, 15, 18 and 21 days). Data are the average of three replicates ± standard error. Identical letters in columns indicate no significant difference (p≤0.05).
Figure 3.
Acid phosphatase extracts of the PSF strains (A. niger AN, P. brevicompactum PB, and P. waksamnii PW) and the control (C), over 21 days of incubation (9, 12, 15, 18, and 21). Data are the average of three replicates ±standard error. Identical letters in the columns indicate no significant differences p≤0.05.
Figure 3.
Acid phosphatase extracts of the PSF strains (A. niger AN, P. brevicompactum PB, and P. waksamnii PW) and the control (C), over 21 days of incubation (9, 12, 15, 18, and 21). Data are the average of three replicates ±standard error. Identical letters in the columns indicate no significant differences p≤0.05.
Figure 4.
Isoenzymatic patterns of in vitro acid phosphatases of the strains (A. niger AN, P. brevicompactum PB, P. waksamnii PW).
Figure 4.
Isoenzymatic patterns of in vitro acid phosphatases of the strains (A. niger AN, P. brevicompactum PB, P. waksamnii PW).
Figure 5.
Soil soluble phosphorus content of coffee (Coffea arabica var. Costa Rica) plants from “San Isidro (A), "Los Bambus" (B), “La Barranca” (C) coffee plantation, in Jilotepec. PSF: Plants inoculated with the phosphorus solubilizing fungus (P. brevicompactum); N-PSF: Uninoculated plants at 60, 120 and 180 days. Data are the average of fifteen replicates ±standard error. Identical letters in the columns indicate no significant differences between plantations (p≤0.05).
Figure 5.
Soil soluble phosphorus content of coffee (Coffea arabica var. Costa Rica) plants from “San Isidro (A), "Los Bambus" (B), “La Barranca” (C) coffee plantation, in Jilotepec. PSF: Plants inoculated with the phosphorus solubilizing fungus (P. brevicompactum); N-PSF: Uninoculated plants at 60, 120 and 180 days. Data are the average of fifteen replicates ±standard error. Identical letters in the columns indicate no significant differences between plantations (p≤0.05).
Figure 6.
Soil soluble phosphorus content of coffee (Coffea arabica var. Costa Rica) plants in the coffee plantation “San Isidro (A), “Los Bambus” (B) and "La Barranca" (C), in Jilotepec. PSF: Plants inoculated with P. brevicompactum; N-PSF: Uninoculated plants at 60, 120 and 180 days. Data are the average of fifteen replicates ±standard error. Identical letters in the columns indicate no significant differences between plantations (p≤0.05).
Figure 6.
Soil soluble phosphorus content of coffee (Coffea arabica var. Costa Rica) plants in the coffee plantation “San Isidro (A), “Los Bambus” (B) and "La Barranca" (C), in Jilotepec. PSF: Plants inoculated with P. brevicompactum; N-PSF: Uninoculated plants at 60, 120 and 180 days. Data are the average of fifteen replicates ±standard error. Identical letters in the columns indicate no significant differences between plantations (p≤0.05).
Figure 7.
Production of cherry coffee beans from plants of Coffea arabica var. Costa Rica of three coffee plantations. PSF: Plants inoculated with the phosphorus-solubilizing fungus P. brevicompactum; N-PSF: Plants without the phosphorus-solubilizing fungus. Data are the average of fifteen replicates ±standard error. Different letters between columns indicate significant differences (p≤0.05).
Figure 7.
Production of cherry coffee beans from plants of Coffea arabica var. Costa Rica of three coffee plantations. PSF: Plants inoculated with the phosphorus-solubilizing fungus P. brevicompactum; N-PSF: Plants without the phosphorus-solubilizing fungus. Data are the average of fifteen replicates ±standard error. Different letters between columns indicate significant differences (p≤0.05).
Figure 8.
Selected coffee plantations of central Veracruz state, Mexico: A) “San Isidro”; B) “Los Bambus” and C) “La Barranca”.
Figure 8.
Selected coffee plantations of central Veracruz state, Mexico: A) “San Isidro”; B) “Los Bambus” and C) “La Barranca”.
Table 1.
fungal strains in scale III.
Table 1.
fungal strains in scale III.
Fungal strain |
Solubilization index |
Aspergillus niger |
2.60 |
1.91 |
1.90 |
|
|
|
|
|
|
Acremonium roseolum |
1.72 |
2.34 |
2.44 |
2.43 |
2.46 |
2.54 |
2.47 |
2.45 |
|
Aspergillus candidus |
2.35 |
2.64 |
2.53 |
2.95 |
2.97 |
2.88 |
2.88 |
2.00 |
|
Aspergillus sclerotiorum |
2.44 |
1.20 |
1.30 |
1.36 |
1.48 |
1.50 |
1.48 |
1.41 |
|
Aspergillus sydowii |
1.80 |
1.75 |
1.66 |
1.63 |
1.59 |
1.39 |
1.32 |
1.14 |
|
Aspergillus sp. 1Y |
1.37 |
1.43 |
1.61 |
1.69 |
1.81 |
1.77 |
1.70 |
1.62 |
|
Cladosporium cladosporioides |
1.59 |
2.27 |
2.72 |
2.61 |
2.60 |
2.58 |
2.36 |
2.54 |
|
Epicoccum nigrum |
1.87 |
2.22 |
2.12 |
2.03 |
1.97 |
1.82 |
1.74 |
1.59 |
|
Eupenicillium euglaucum |
2.00 |
2.39 |
2.51 |
2.58 |
2.73 |
2.82 |
2.82 |
2.86 |
|
Eupenicillium ludwigii |
3.53 |
3.08 |
2.61 |
2.64 |
2.65 |
2.65 |
3.05 |
2.91 |
|
Fusarium sp. C25 |
2.80 |
2.76 |
2.68 |
2.67 |
2.67 |
2.48 |
2.34 |
2.19 |
|
Fusarium sp. 3Y |
2.50 |
2.42 |
2.44 |
2.34 |
2.27 |
2.05 |
1.96 |
|
|
Humicola sp. 2gh205 |
2.14 |
2.01 |
1.79 |
1.76 |
1.72 |
1.69 |
1.72 |
1.55 |
|
Merimbla sp. 3gh18 |
1.76 |
1.75 |
1.76 |
1.72 |
1.63 |
1.59 |
1.54 |
1.77 |
|
Penicillium arenicola |
1.42 |
1.74 |
1.77 |
2.02 |
1.68 |
1.63 |
1.41 |
1.31 |
|
Penicillium brevicompactum |
2.47 |
2.96 |
3.37 |
3.61 |
3.36 |
3.11 |
2.94 |
2.64 |
|
Penicillium glabrum |
1.47 |
1.70 |
1.72 |
1.62 |
1.64 |
1.53 |
1.39 |
1.35 |
|
Penicillium miczynskii |
2.26 |
2.09 |
1.94 |
2.17 |
2.70 |
1.96 |
1.97 |
1.72 |
|
Penicillium olsonii |
1.82 |
1.98 |
2.00 |
1.93 |
1.87 |
1.77 |
1.68 |
1.67 |
|
Penicillium verrucosum |
1.43 |
1.93 |
1.99 |
2.07 |
1.86 |
1.61 |
1.47 |
1.34 |
|
Penicillium waksmanii |
1.76 |
2.80 |
3.20 |
3.60 |
3.67 |
3.88 |
3.83 |
3.79 |
|
Penicillium sp. 90 |
2.13 |
2.20 |
2.12 |
2.16 |
2.05 |
2.12 |
2.05 |
1.85 |
|
Sagenomella diversispora |
2.83 |
2.93 |
3.23 |
3.10 |
3.15 |
2.95 |
2.83 |
2.63 |
|
Scopulariopsis brevicaulis |
1.98 |
2.77 |
2.95 |
2.76 |
2.61 |
2.66 |
2.30 |
2.16 |
|
Talaromyces flavus var. flavus |
3.52 |
2.66 |
2.02 |
2.00 |
2.12 |
2.14 |
2.30 |
2.21 |
|
Trichocladium asperum |
2.43 |
2.87 |
2.85 |
3.00 |
3.34 |
3.15 |
3.33 |
3.00 |
|
Table 3.
Geographic location, elevation, and characteristics of the study sites.
Table 3.
Geographic location, elevation, and characteristics of the study sites.
Sites |
Annual mean precipitation |
Latitude |
Longitude |
Elevation (masl) |
Mean temperature |
Management type |
Soil type |
San Isidro |
241 |
19°36’42.74’’ |
96°56’16.01’’ |
1370 |
22 |
Traditional polyculture |
Andosol |
Los Bambús |
275.9 |
19°36’38.07’’ |
96°55’40.57’’ |
1414 |
25 |
Traditional polyculture |
Andosol |
La Barranca |
298.2 |
19°36’12.15’’ |
96°54’44.91’’ |
1484 |
25 |
Traditional polyculture |
Andosol |
Table 4.
Physico-chemical characteristics of the coffee plantations evaluated.
Table 4.
Physico-chemical characteristics of the coffee plantations evaluated.
|
Coffee plantations |
|
“San Isidro” |
“Los Bambus” |
“La Barranca” |
pH |
6.11 |
6.69 |
5.43 |
Retained P |
87.35 |
89.8 |
81.63 |
Organic material |
12.46 |
3.93 |
4.72 |
Organic carbon |
7.23 |
2.28 |
2.74 |
Cation exchange capacity (CEC) |
27.09 |
20.88 |
21.51 |
field capacity (FC) |
31.72 |
22.69 |
21.62 |
Bulk density |
0.893 |
1.016 |
0.994 |
Clay |
29.8 |
45.8 |
49.8 |
Silt |
30.56 |
22.56 |
28.56 |
Sand |
39.64 |
31.64 |
21.64 |
Texture |
Clay loam |
Clay |
Clay |
Fe |
69.38 |
111.63 |
163.03 |
C |
8.5 |
2.9 |
3.5 |
N |
0.72 |
0.27 |
0.27 |