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Chacón, G., D. Gagnon and D. Paré. 2016. Quinoa biomass production capacity and soil nutrient deficiencies in pastures, tree plantations and native forests in the Andean Highlands of Southern Ecuador. La Granja: Revista de Ciencias de la Vida. Vol. 24(2):16-28. ISSN: 1390-3799.

1 Introduction

Land-use patterns in the Neotropics in general, and in the Andes in particular, are experiencing a shift towards pasturing for cattle ranching, specifically dairy cattle in the Andean highlands. This shift in land-use patterns responds to changes in unbalan- ced social structures, market conditions, access to farmland and rural emigration (Jampel, 2016). In Andean Ecuador, the situation is no different from the rest of the region and the local rural economy is largely based on a dairy cattle livelihood, whereas most of the agriculture is dedicated to the production of agro-alimentary goods for export according to massive urban demands within or outside the country (Bretón, 2008; Potthast et al., 2012). Cattle ranching has developed at the expense of Andean montane rainforests and perennially humid páramo grasslands, above the tree line, through slash and burn practices for conversion to pastures. Both types of ecosystems have high biodiversity and pro- duce several ecosystem services, such as water retention and water regulation for the main cities of Ecuador and rural populations (Harden et al., 2013). Not only pastures, but also cultivated lands and tree plantations cause increased streamflow variability and significant reductions in catchment regula- tion capacity and water yield (Ochoa-Tocachi et al., 2016).

In the Andean highlands of southern Ecuador, steep slopes, high precipitation regimes, water erosion and the lack of proper soil management (which depends exclusively on externalities rather than using and increasing the supply of locally produced and renewable soil fertility resources such as manure, cover crops, compost and optimizing nutrient use efficiency throughout the farm, according to Fonte et al. (2012), pasture soils experience progressive degradation linked to soil N and P depletion; after soil degradation pasture lands are ulti- mately abandoned. On these abandoned pastures, or on natural páramo grasslands, Pinus patula Sch-lecht. is used in monospecific plantations at a wide range of elevations up to 3.400 m.a.s.l. Eucalyptus globulus Labill. is also used in plantations, but at lower elevation ranges (maximum upper limit of aprox. 2.800 m.a.s.l.). These two exotic tree species are largely preferred in local forestry plantations because of their fast growth and timber production. However, these plantations, through the effect of their litter, can also cause a decrease in soil pH and soil cation concentrations (Chacón et al., 2009; Farley et al., 2012; Harden et al., 2013).

Within this scenario of land-use patterns in thehighlands of Southern Ecuador, a growth responseexperiment was conducted on soils from pastures,P. patula and E. globulus plantations, compared tosoils of native Andean forests, using quinoa, Cheno podium quinoa Willd., as a test crop species, andwithfertilization treatments with three fertilizers (N alone,P alone, and a combination of N + P). In Ecuador,quinoa was already used in pre-Inca times, althoughits cultivation declined in the Andes followingthe Spanish conquest (circa 1539 AD). Quinoahas been largely replaced by corn as an importantstaple-crop, but as opposed to corn it is adapted toacid soil conditions generally found in Andean regions(Risi and Galwey, 1989; James, 2009). The specificobjectives of this study were:

1. 1. to identify which land-use types (pastures, two tree plantations and native forests) are most likely to reduce soil fertility;

2. 2. to examine which soils from the four land-use types produce the lowest growth of quinoa; and,

3. 3. which soil nutrients are most affected by the four land-use types.

2 Materials and methods

2.1 Soil sampling and experimental design

Soils of each land-use types were sampled at fourseparate locations within a wide area of southernEcuador (Chacón et al., 2015). The four land-use typeswere second growth native forests (Nf), pastures(Pa), P. patula plantations (Pp), and E. globulus plantations (Eg) (Figure 1). These land-use typeswere located in areas of similar elevation, at approximately 3.000ma.s.l. (Figure 1), and similar annualprecipitation regimes (between 1050 and 1700mmin regions 1 and 2, and between 660 and 1100mmin regions 3 and 4) (Figure 1). Following a north south direction, soils change from Histic Andosolsin regions 1 and 2, to Dystric Histosols in regions 3 and 4, according to annual rainfall, the influence ofvolcanic ash or to a lower soil Al and Fe content respectively (Buytaert et al., 2006; Celleri et al., 2007); ineither case, these soils developed on pyroclastic materials, lack allophane, have high C and organic. matter content and low bulk density, and are generally classified asGroup 4–Andosols (IUSS Working Group WRB, 2015). In each of the land use types,a 20m×20m plot was established. Within each ofthe plots, 0.05m3 of soil was collected from the first20 cm of surface soil. Soil samples were transported to a common garden in the Mazán region (Figure 1).

Soil samples were sieved through a 1 cm mesh to remove large non-soil parts. Plastic pots were filled with 4 L of soil. A portion of soil per pot was taken to the laboratory for chemical analyses. A nested randomized block design was established so that each of the four regions corresponded to each of four blocks (Chacón et al., 2015). Within each of the blocks, each of the four land-use types of soils were divided in four sub-units (four pots) and subjected to four treatments (control, N, P, and N+P fertilizers).This design produced 16 randomly distributedcombinations of four treatments per block (fourblocks = replicates), giving 64 experimental units.Subsequently, six quinoa seedswere planted in eachof the pots, and only two germinated seedlings wereleft to grow. Fertilizer treatments were made oncea week during 98 days.N-fertilized soils receivedweekly additions of 175mg N as ammonium nitrate(NH₄NO₃). P-fertilized soils received weekly additionsof 110mg P and 65mg Ca as triple superphosphate[Ca(H₂PO₄)2H₂O]. NP-fertilized soils receivedweekly 87.5mg N, 55mg P and 32.5mg Ca(half of ammonium nitrate and triple superphosphate combined fertilizers) (Chacón et al., 2015).

Table 1. Comparison of soil properties before bioassay with quinoa. In parentheses: CV in%. Different letters represent significant differences at P ≤ 0.05. Table is reproduced from Chacón et al. (2015).

2.2 Laboratory and data analyses

The two quinoa plants per pot were harvested andwashed, taken to the laboratory and oven dried at 50^◦C for 72 hours. Plants were weighed for dry biomass.Analyses of total N, P, K, Ca and Mg in planttissues followed an acid-hydrogen peroxide digestion procedure (Allen, 1989). For the soil samples, were extracted with KCl 2M and analyzed according to Maynard and Kalra et al.,(1993). Exchangeable cations were extracted with BaCl₂ 0.1M and analyzed according to Hendershotet al., (1993). The effective cation exchange capacitywas calculated by adding all cations. Pwas extracted by the method of Bray II and analyzed according to McKeague (1978). The percent soil organic matter was estimated by loss on ignition (Grimshaw, 1989). Soil pH was determined with aglass electrode from a 1:2 soil: water solution.

A nested ANOVA and a Tukey means comparisontest were used for all variables after normality of data was confirmed. All statistical analyses weredone using SAS (SAS Institute, 2008).

3 Results and discussion

3.1 Comparison of soil properties

In the initial soil samples from the four land-use typesacross four regions, statistically significant differenceswere found for the soil variables that arelinked to the pH. The Al concentration in pine soilsplaces Al in these soils at the toxic levels (>60%) reportedby Cochrane T. T. y P. A. Sanchez (1982), while Ca can be seen as deficient compared to the othersoils (Tables 1 and 2). This pattern is associated with differences in pH, and the general low base status ofpine soils in the Ecuadorian Andes and under Pinus patula plantations in the same region as this study (Farley and Kelly, 2004; Chacón et al., 2009). However, this pattern is different in the other soils. Generally, the lower pH values and higher ECEC andcation concentrations found in native forest soils arenot consistent with the higher pH values and lower ECEC and cation concentrations found in pastureand eucalyptus soils. The effect of soil organic matter,through its humic and fulvic acids, and the effectof a higher Al and Fe content in native forestsoils may have decreased soil pH, although the highe rbase status of these soils probably offers a truerassessment of their fertility (Table 2).

Table 2. Comparison of final soil properties after conclusion of bioassays with quinoa (this study) and corn (Chacón et al., 2015). Soils from both bioassays were analyzed separately but combined for this table because values and statistical significance were nearly identical (n = 8).

Nutrient depletion at a critical level was foundfor high elevation volcanic soils in northern Ecuador;a minimum soil level of 12 ppm is generallyrequired for adequate growth of agriculturalproducts (Espinosa, 1992). Except for soils inthe P and NP-fertilizer treatments, all soils fall belowthese levels, with native forest soils having ahigher content, and pasture and eucalyptus soils having a lower content in the C- and NP treatments.Thus, the soils used in the experiments reported here can all be considered as deficient.Evidence suggests that levels decrease when is fixed by reactions with Fe and Al inacid soils (Smethurst, 2010). Pine soil contentwas no different from the other soils in spite of a lowerpH. availability in pine soils may be alsorelated to mycorrhizal activity, which can en hance the weathering rates of from the bound pools (Allen, 1991).

The lack of statistical differences, especially inthe N-treatment, implies that all soils responded similarlyto N additions (Table 2), and that the differencesin initial values areless important in determining specific differencesamong the four land-use type soils. The only clearpattern, probably very variable in time, is that pineand native forest soils tend to have higher amountsof than pasture and eucalyptussoils. This trend is clearer if we add together values. Increased availability of Nand has been reported in other coniferous forests,although N deficiencies can appear in secondor more rotations (Crous et al., 2011). In initial soilsamples was the dominant form in all soils.However, after the bioassay, was considerablyincreased and decreased, suggesting that nitrification had occurred, perhaps caused by some form of incubation process in the bioassay pots. N mineralization experiments with volcanicsoils in Costa Rica (Montagnini and Sancho, 1994) also revealed enhanced nitrification in incubations.

In normal conditions, nitrification in our soilsshould be limited by the acidic pH found more generallyin pine soils. Further evidence is the predominance of over in pine soils in the N- and NP-treatments, whereas values were equivalent in native forest soils, and had become predominant in pasture andeucalyptus soils. This highlights the potential for Nmineralization in native forest soils, and the role ofhigher pHvalues in pasture and eucalyptus soils, as well as the problem of lower pH in pine soils. However, N mineralization during the bioassay in thisstudy was not significant because the sum of was similar to the sum of initial soilvalues. Therefore, in natural conditions, we confirmed the patternsvseen else where showing that nitrificationis inhibited by acidic soil conditions andby the amount of available , which is the principal control for nitrification in most humid tropicalecosystems (Vitousek et al., 2010).

Generally, N concentrations (and concentrations)in our sample soils was limited becausesoil productivity was generally decreased. The low availabilitymight be limiting N mineralization from organic matter (Munevar and Wollum, 1977).Percent SOM was high, statistically comparable inthe samples, and unaffected by any of the treatments.Inmontane tropical soils the decay of humusin the mineral soil is slow (Jenny, 1950) because oflow temperatures, low pH, water-logging and litterquality, which results in high SOM accumulation (Oades et al., 1989). Nevertheless, changes of a fewpercent in soil organic matter can have important effects on the soil nutrient status and on plant nutrition, which was shown in Andisols from the lowermontane rain forest zone in southern Ecuador (Davidson et al., 1999). In this study, SOM in nativeforest and pine soils averaged 39.9% and 36.6% respectivelyas opposed to 29.9% found in pasture and eucalyptus soils. The humus-rich (high SOM) Andisols contain high amounts of humic acid (Nanzyo et al., 1993). This may explain the low pH foundin native forest and pine soils compared to pastureand eucalyptus soils. Under cultivation, carbonand organic matter is lost (Ewel et al., 1991) whichmay explain the loss of SOM in pasture and eucalyptussoils, since it is very likely that cultivation hadbeen the previous land use of these soils (Chacón et al., 2009). However, in pine soils SOM may haveaccumulated because of low decomposition ratesdue to the litter’s high lignin content (Taylor et al.,1989). Comparing native forest and pine soils, fertilitymay be largely dependent upon the quality andnot the quantity of SOM, which would cause differentmineralization rates due to different types oflitter inputs to the forest floor. Except for Ca, Al, pHand the limitations of N and P, the other soil propertiesmeasured in this study tend to reflect thecharacteristics of volcanic ash derived soils ratherthan the effects of the current vegetation as shownelsewhere (Chacón et al., 2015).

Table 3. Percent mortality of quinoa after bioassay on soils from four land-use types and under four fertilizer treatments.

3.2 Fertilizer treatment effects on soil properties

The effects of N additions are reflected in the patternseen for soil pH. Whether in the N- or combinedNP-treatments, pH values were always significantlylower in all soils except in native forest soils.We interpret this as the result of H+ released duringnitrification of from the ammonium nitratefertilizer (Table 2). All N-fertilizers are largely convertedto thus acidifying the soil (Wild, 1989; Oskarsson et al., 2006). In the P-treatment, content was always higher than , suggestingthat increased N mineralization from organicmatter, but the amounts of P added were too low toproduce significant differences (Table 2). In volcanicsoils from Colombia, sampled from similar elevationsas in this study, additions of large quantities of Ca(H₂PO₄)₂.H₂O increased N mineralization ratesby enhancing the use of soil carbon by microorganisms (Munevar and Wollum, 1977). Ammonium,ammonium nitrate, urea (Finck, 1982) and poultrymanure have been considered as acidifying fertilizers.We can conclude that fertilizer applicationsin the studied soils should include and Ca as well, in order to increase pH and to enhance SOM mineralization.

Findings suggest that these soils depend moreupon inorganic fertilization rather than naturalP mineralization. In fact, fertilizer experiments insoils taken from the highlands of northern Ecuador (Espinosa, 1992) have also found incrementsand enhanced yields of agricultural crops. In Costa Rica, inorganic P fertilization increased the mineralizationof organic P as opposed to the reduction of the P pools through organic additions (Paniagua et al., 1995). There was a pattern of increased pHin soils that received P additions, more visible ineucalyptus and pine soils than in native forest andpasture soils. Soil pH in the P-treatmentwas alwayshigher than in the control treatment, but was lowerthan the pH measured in initial soils samples (Tables1 and 2). This is most likely the effect of theamounts of Ca present in the triple-superphosphateutilized as P-fertilizer rather than alone. Theuse of lime can alleviate Al toxic levels by neutralizingsoil acidity in volcanic ash soils (Shoji et al.,1993). In Costa Rican acid soils, CaSO₄ and CaCO₃ reduced Al toxicity; the latter also raised pH values,although neither fertilizer had significant effects onK and Mg (López and González, 1987). The additionsof Ca in this study had no significant effectson the soil concentrations of other cations suggestingthat the level of Ca added was low, althoughsufficient to raise soil pH and to lower Al content inpine soils.

3.3 Quinoa growth, biomass and the effects of fertilizer treatment

The overall quinoa mortality was generally distributedasN (38%) >C (28%) >NP (22%) >P (0%) (Table 3). Quinoa 100% survival occurred only in eucalyptussoils and in the P-treatment across the fourland-use types. In a few cases, only one of two quinoaseedlings survived per pot. Only one seedlingsurvived in pine soils under control and N-P treatmentsin only one block. In the other soils and treatmentswhere mortality was present, the two plantsper pot died (Table 3). The negative effect of Pinus patula plantations soils is clearly shown byquinoa mortality in all treatments (control included),except in the P-treatment. Quinoa died in thecontrol (25%) and N (50%) treatments of native forestsoils, suggesting an effect of lower soil pH,which was reduced with Ca additions in the P and NP-treatments (Table 3). In pasture soils, quinoamortality was 25% in the NP-treatment, although there was nomortality in the N- or other treatments,andmight be explained by the accidental loss of oneplant (grasshopper damage) rather than a soil problem(Table 3). Quinoa mortality was significantly decreased by P additions, P more than NP perhapsbecause of an acidifying effect of the N fertilizer accordingto Oskarsson et al., (2006). Mortality wasincreased by N additions in pine soils to the pointwhere all quinoa plants died in the N-treatment andnone in the P-treatmentwith respect to control soils,suggesting a stronger P limitation and perhaps alower pH, K and Ca as principal factors controllingmortality in pine soils. This also suggests thatquinoa is more sensitive to soil nutrient deficienciesthan corn (Chacón et al., 2015) (Table 4). Thismortality, as well as the higher coefficients of variationfor native forest soil nutrients have reducedthe number of statistically significant differences inquinoa biomass production, and nutrient contents,among the four land-use type soils. Generally, quinoagrowth responded to P and NP-fertilizers insoils excluding those from the pine plantations (Tables 2, 3 and 4). There was no response in the N treatmentand growth was very similar to the onefound in control soils. The combined effect of N and P significantly increased corn and quinoa biomasses.Thus, N and P are limiting in these soils, but Pis the primary limiting factor. The same is true fornutrient contents (Table 4).

The very low biomasses produced by all controlsoils indicate a loss of agricultural potential throughthe reduction of soil fertility, which has lead to fertilizationdependency to sustain crop production.For example, experiments with potatoes on EcuadorianAndisols required P applications every cycleto obtain adequate yields (Espinosa, 1992). Quinoa growth started to be consistently poorer in pinesoils just as growth began to respond to fertilizationin the other soils. This suggests that pine soils arefurther limited by soil factors other than N or P limitation alone.

It is not proven that N and P supply was limitedin pine soils because of the generally higher amounts of N and P present in these soilswhen compared to pasture and eucalyptus soils.The trends seen for increased quinoa biomass andnutrient contents were too small to be statisticallysignificant. Specifically, the contents of P, K, Ca and Mg increased with P additions as opposed to N additions.One hypothesis is that P concentrations regulate Ca and Mg uptake by controlling the effluxpump in crops (Blevins, 1994). At low P concentrations,effluxes of Mg and Ca were reported fromroots in wheat and tall fescue crops (Reinbott and Blevins, 1991). In pine soils, the effect of Ca in the P-fertilizer treatment was to reduce soil acidity, and perhaps Al toxicity, and is likely to have improvedquinoa growth, althoughwe cannot separate it fromthe direct effect of P.However, pine soil deficiencies,especially K and Ca, were not eliminated to attainbetter growth. We can observe large increases of Kcontent in quinoa, with the P- and NP-treatments inpasture and eucalyptus soils (Table 4).

As for soil properties, the differences in quinoabiomass production and nutrient content are betterobserved between the group of native forest, pastureand eucalyptus soils and of pine soils alone,which always produced lower biomasses and nutrientcontents, and an thus be considered to havelower productivity and fertility than all the othersoils. Eucalyptus soils produced higher quinoa biomassin the P-treatment, suggesting a further P limitationfor this species in these soils as opposed,for example, to corn (Chacón et al., 2015).Quinoa K,Ca and Mg contents, similar in native forest, pastureand eucalyptus soils, were generally higher thanthe one produced on pine soils in the P-treatment,suggesting that K, Ca and Mg supply to quinoawas equivalent in all soils except for pine soils, andhighlights the lower K, Ca and Mg contents in pinesoils. Because quinoa had 100% mortality in the Ntreatmenton pine soils, quinoa biomass, N, Ca and K contents after growth on pasture soils were significantlylower than in native forest soils, evidencethat may indicate that N is more limiting in pasturesoils than in the other soils.

Apart from the identified nutrient limitations togrowth such as P for all soils (except perhaps pinesoils), N specifically in pasture soils, and K and Ca coupled with a lower pH in pine soils, the magnitude of growth responses to nutrient enrichment,especially among native forest, pasture and eucalyptussoils is linked to the fact that all land-use typeswere subjected to past impacts that have lowenutrient requirements of quinoa. The assessmentof specific nutrient limitations to plant growthvaries depending on the species selected. Quinoaseemed more sensitive to nutrient limitations thancorn (Chacón et al., 2015), however, quinoa is reportedto grow in the Andes from sea level to 3.800m.a.s.l., in marginal areas with poor (Risi and Galwey,1989), acid soils (pH = 4.5 in Cajamarca, Peru),both sandy or clayey soils (Mujica, A, 1994), where N influences the growth of quinoa. Evidence fromthis study suggests that despite the fact that quinoacan adapt to severe climatic conditions, soils of southern Andean Ecuador are currently not able tosupport the production of this crop without additionsof combined fertilizers containing P, N, K and Ca as the principal elements. Corn remains an easiercrop to grow (Chacón et al., 2015), in terms of soil requirements,and this may largely explain why it hasreplaced quinoa as a major Andean crop, as historic land-use effects have generally reduced soil fertility.

Agradecimientos

4 Acknowledgements

We gratefully acknowledge the Universidad delAzuay and ETAPA for providing laboratory facilities,equipment and logistics. We also wish to acknowledgethe Biodôme de Montréal and MacdonaldCollege (McGill University) for providing facilitiesfor soil and plant tissue analyses.

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Notas de autor

¹ Escuela de Biología, Ecología y Gestión, Universidad del Azuay, Av. 24 de Mayo 7-77,Teléfono: (593) 74091000, fax: (593) 72815997, Cuenca, Ecuador.

² Department of Biology, Faculty of Sciences, University of Regina, 3737 Wascana Parkway, S4S 0A2; teléfono: (306) 3372110,fax: (306) 5854291, Regina, Saskatchewan, Canada.

³ Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, G1V 4C7; teléfono: (418) 6487598; fax: (418) 6485849, P.O. Box 3800, Sainte-Foy, Quebec, Canadá.

Enlace alternativo

http://revistas.ups.edu.ec/index.php/granja/article/download/24.2016.02/1136 (html)