Introduction

The silvopastoral systems (sps) are characterized as agroforestry arrangements that include shrubs, trees or timber species together with a herbaceous component generally associated with grasses (^{Pezo & Ibrahim, 1998}; ^{Sinclair, 1999}), which can range from intensive (> 10,000 shrubs/ha) without widespread tree cover (^{Calle et al., 2013}), up to multistratified with low density (< 100 trees/ha) and widespread tree cover (^{Cajas-Giron & Sinclair, 2001}).

In the case of multi-stratified systems, the facilitating interactions (reduction of evapotranspiration, nitrogen fixation, among others) and competition (water, light and nutrients) between the arboreal and the herbaceous components are essential elements in the sustainability and productivity of the system (^{Dohn et al., 2013}; ^{Guenni, Seiter, & Figueroa, 2008}; ^{Martínez, Cajas, León, & Osorio, 2014}), especially under grazing conditions. However, sometimes the potential for herbaceous productivity in SPS with tree cover becomes limited by the shadow effect (^{Abraham et al., 2014}; ^{Paciullo et al., 2017}). Usually, intercepts of incident radiation above 50 % may affect the production of biomass in tropical grasses (^{Guenni et al., 2008}; ^{Paciullo et al., 2017}; ^{Villanueva, Ibrahim, & Ríos, 2008}), due to the reduction in the photosynthetic rate, especially in C4 species (^{Dohn et al., 2013}; ^{Santiago-Hernández et al., 2016}).

The interactions between ca nopy cover and the productivity of herbaceous species are not entirely linear, particularly in grass species that may exhibit morphological and adaptive plasticity attributes (^{Abraham et al., 2014}; ^{Guenni et al., 2008}). This term has been described as the ability of some plants to change biochemical, morphological and physiological attributes, in response to temporary or permanent environmental variations (^{De Kroon, Huber, Stuefer, & Van Groenendael, 2005}; ^{Dias-Filho, 2002}). According to Guenni et al. (2008), these adaptations are mostly associated with respiratory rate reductions, increases in the aerial/root component relations, and increases in the specific leaf area.

In this sense, other authors have also cited leaf stretching (^{Paciullo et al., 2017}), the reduction in the appearance rate of stems, and increases in their length (^{Abraham et al., 2014}).

In grasses (Poaceae) of the genus Megathyrsus, evidence of adaptive plasticity has been reported under tree shade conditions, with an increase in morphological attributes such as plant height, leaf width, length and stem appearance rates (^{Medinilla-Salinas et al., 2013}; ^{Paciullo et al., 2017}; ^{Santiago-Hernández et al., 2016}; ^{Silveira, Dos Santos, Rodrigues, Rodrigues, & Alencar, 2017}; ^{Viafara, Clavero, & Araujo-Febres, 1997}), as well as biochemical attributes such as increases in crude protein content (^{Durr & Rangel, 2003}; ^{Paciullo et al., 2017}; ^{Santiago-Hernández et al., 2016}).

The behavior of the herbaceous component under tree cover conditions in a SPS is a fundamental part of its success and adoption. However, there is still little knowledge about the potential of grasses in sps with tree cover and light restriction (^{Silveira et al., 2017}).

The current study aimed to compare the bromatological and structural behavior of Megathyrsus maximus ( Jacq.) B.K. Simon & S.W.L. Jacobs (Poaceae), under four multi-strata silvopastoral arrangements and a meadow without trees.

Materials and methods

Study area

The evaluation was carried out at the Turipaná research center linked to Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA), located in Cereté, Córdoba, Colombia (08°51' N, 75°49' W; 18 m.a.s.l.). The area is located in the Caribbean region and has two defined climatic periods: a rainy season that occurs from May to November and a dry one from December to April. The average annual rainfall is 1,380 mm, with an average annual temperature of 28 °C. During the year, potential evapotranspiration of 1,240 mm and a relative humidity of 81 % were recorded (data from the AGROSAVIA-Turipaná climatic station). According to the life zones classification of Holdridge (1971), the area is categorized ecologically as tropical dry forest (bs-T).

In 1998, four types of silvopastoral systems of different structure and complexity, as well as a treeless meadow (control) were established (^{Cajas-Giron & Sinclair, 2001}). The silvopastoral arrangements consisted of three different strata: pastures, shrubs, and trees (for fruit or timber production). The control treatment (meadow) consisted only of pastures (Cynodon nlemfuensis Vanderyst, Dichanthium aristatum (Poir.) C. E. Hubb., and Megathyrsus maximus). The first silvopastoral arrangement (p-Arbust) included only shrubs: Leucaena leucocephala (Lam.) De Wit. and Crescentia cujete L.; the second included a stratum of trees (p-Arbor): Cassia grandis L. F., Pithecellobium saman ( Jacq.) Benth., and Guazuma ulmifolia Lam.; the third had a combination of pastures, shrubs, and trees (p-Arbust-Arbor); and the fourth arrangement (p-Arbust-Arbor-Mad) included the previous strata plus the inclusion of timber species: Pachira quinata W.S. Alverson and Swietenia macrophylla King (table 1).

The experiment was carried out in an area of 30 ha divided by a differential drainage effect in three sectors characterized as blocks (poor, moderate and optimal drainage). In each block, a replicate of the evaluated treatments was established in an area of 2 ha (100 m wide by 200 m long), for a total of three replicates per treatment and 15 plots (figure 1). Each treatment was divided into five strips of 4,000 m² subject to a grazing scheme of 2 days of occupation and 28 days of rest.

Source: Elaborated by the authors employing a satellite image of DigitalGlobe® Google 2019. Photograph at 1,338 m abovethe terrain.

Figure 1. Satellite image of the spatial distribution of the silvopastoral systems assessed in CI Turipaná (agrosavia), Cereté (Córdoba, Colombia). Block 1: orange; block 2: red, and block 3: yellow. 

Table 1. The botanical and structural composition of the silvopastoral arrangements and the treeless meadow assessedin CI Turipaná, Cereté (Córdoba, Colombia) during 2011 

Source: Adapted from Barragán-Hernández, Mahecha-Ledesma and Cajas-Girón (2015)

Results and discussion

The treatment significantly affected (p < 0.05) the proportion of CP in M. maximus. The average CP in the Pasto and p-Arbust treatments (without tree coverage) was 2.42 percentage points lower compared to the average values found in the p-Arbor, p-Arbust-Arbor and p-Arbust-Arbor-M treatments (with tree coverage). In the case of the fibers, an effect (1 < 0.05) of the season was observed on the neutral and acid detergent fibers. The ndf and the adf for the dry period were higher (65.16 % and 37.30 %, respectively) compared to the values registered in the rainy period (63.28 % and 37.30 %, respectively). As expected, age significantly affected all the variables evaluated (p < 0.05), with an increase for fibers and a decrease in protein and in situ dry matter digestibility, from 7 to 28 days (table 2).

Table 2. Bromatological composition in percentages of Megathyrsus maximus in four silvopastoral arrangements and a meadow without trees, in CI Turipaná during 2011 cp: Crude protein; ndf: Neutral detergent fiber; adf: Acid detergent fiber; isdmd: In situ dry matter digestibility; sem:Standard error of the mean. 

Source: Elaborated by the authors

^Note:Different letters between averages in the same column indicate significant statistical difference at p < 0.05, according tothe Tukey test.

The interaction effect of the treatment and age was observed (p < 0.05) for the CP variable. All the treatments show a decreasing tendency for cp content as age advances. However, the trend is more accentuated in the Pasto and p-Arbust treatments (without tree cover), compared with the p-Arbor, p-Arbust-Arbor and p-Arbust-Arbor-M treatments (with tree cover). In day 14, the results obtained for CP differs significantly between the group of treatments with and without tree coverage (figure 2).

Table 3 illustrates the structural behavior of M. maximus evaluated according to four silvopastoral arrangements and the treeless meadow. The treatment significantly affected (p < 0.05) plant height, LSR and leaf width. The p-Arbor treatment showed the highest average height per plant (80.2 cm), which significantly exceeded (p < 0.05) the average height recorded in the Pasto treatment (68.8 cm). This behavior was consistent with the leaf width variable, finding the broadest leaf values in the p-Arbor and p-Arbust-Arbor treatments (2.68 cm and 2.71 cm, respectively) with a significant difference compared to the Pasto treatment (2.16 cm). The LSR variable showed a contrary trend to the variables described above. The Pasto treatment registered the best leaf: stem ratio with 51.7 g of leaves per gram of stem. This record was significantly different (p < 0.05) from the records reported in the treatments with arboreal coverage, i.e., p-Arbor (16.6 g), p-Arbust-Arbor (13.6 g) and p-Arbust-Arbor- M (16.5 g).

Nonetheless, the season significantly affected (p < 0.05) leaf height and width. In the dry season the highest plant height (79.89 cm) and, on average, the widest leaf (2.61 cm) was obtained, compared to the rainy period (70.19 cm and 2.41 cm, respectively).

Source: Elaborated by the authors

Figure 2. Effect of the silvopastoral arrangement and age on the crude protein content of Megathyrsus maximus, in ci Turipaná during 2011. Cob = Tree cover; SinC = No tree cover. Vertical bars indicate the standard error of the mean. 

Table 3. Structural characteristics of Megathyrsus maximus in four silvopastoral arrangements and a meadow without trees, in CI Turipaná during 2011 lsr: Leaf: stem ratio; sem: Standard error of the mean. 

Source: Elaborated by the authors

^Note:Different letters between averages in the same column indicate significant statistical difference at p < 0.05 according tothe Tukey test.

The interaction of the SPS arrangement, the age and the season showed a significant effect (p < 0.05) on plant height and leaf width. The height for the dry period at 28 days was higher in the SPS arrangements p-Arbor (104.77 cm), p-Arbust-Arbor (102.62 cm) and p-ArbustArbor-M (111.31 cm), compared with treatments without tree cover (86.39 cm in p-Arbust and 70.97 cm in Pasto). Further, leaf width showed similar behavior to plant height. During the dry period after 28 days of regrowth, the SPS arrangements with tree cover registered the highest averages leaf width values (2.80, 2.81 and 2.74 cm for p-ArbustArbor-M, p-Arbust-Arbor and p-Arbor, respectively), compared with the Pasto and the p-Arbust treatments, which recorded an average leaf width of 2.1 and 2.3 cm, respectively (figure 3).

Source: Elaborated by the authors

Figure 3. Effect of the silvopastoral arrangement and the age in some structural characteristics of Megathyrsusmaximus, in ci Turipaná during 2011. Cob = Tree cover, SinC = No tree cover. Vertical bars indicate the standarderror of the mean. 

The compositional and morphological changes observed in M. maximus are consistent with the descriptions reported for C4 species under shade (^{Sage & McKown, 2006}). C4 plants, such as M. maximus (^{Giraldo-Cañas, 2010}) have evolved to adapt to highly luminous and hot environments with low CO₂ saturation, through biochemical and anatomical modifications that focus on carbon fixation in the RuBisCO enzyme (^{Edwards & Smith, 2010}). However, the plasticity of C4 plants to shade conditions revolves around the carbon economy, in which the plant increases its photosynthetic efficiency by increasing the leaf area, decreasing leaf thickness, by changing the aerial/root proportions and increasing chlorophyll concentration. All these changes are mediated by nitrogen availability (^{Valadares & Niinemets, 2008}), which can be influenced by the presence of leguminous trees (^{Pentón & Blanco, 1997}).

In this work, the bromatological changes of M. maximus under shade were evident, mainly for cp, with a difference of at least 2.4% between the SPS with tree cover and the p-Arbust and Pasto treatments. Authors such as Paciullo et al. (2017) report increases in cp content for M. maximus in 3.3 % under artificial shade conditions (up to 58 % retention with black polypropylene cloth); moreover, Santiago et al. (2016) recorded increases in leaves of 2.5 % in CP and 0.8 % in stems under the coverage of Melia azedarach L.

On the other hand, Durr and Rangel (2003) reported increases of 4.7 % in cp content under the shade of Pithecellobium saman. Contrary to this, when Obispo, Espinoza, Gil, Ovalles and Rodríguez (2008) evaluated shadow levels between 10 % and 30 % generated by P. saman, they did not report a significant effect of the shadow on CP content in M. maximus, like Medinilla et al. (2013) under coverage of Gliricidia sepium ( Jacq.) Kunth ex Walp.; the latter was probably influenced by the decrease in organic carbon contents in the soil during the experimental period.

Regarding the increase of cp in sps, Cruz (1997) has reported that nitrogen increases in the grass under tree shade are associated to phenomena such as the recycling of nutrients through the fall of litter and the facilitation of nitrogen promoted by legumes species. Moreover, Martínez et al. (2014) evaluating the sps arrangements object of the current study reported that under the arrangements with tree coverage (p-Arbor, p-Arbust-Arbor, and p-Arbust-Arbor-M), the nutrient recycling dynamics improve the contents of P, K, Ca and organic matter, compared with the meadow without trees.

Also, authors such as Abule, Smit and Snyman (2005), through the evaluation of the influence of trees on plant composition and soil nutrients, have created the term "fertility island" to describe the improvements of nitrogen and organic matter under tree canopies generated by the interaction between soil microfauna and the accumulation of litter. In this sense, Avendaño-Yanez, López-Ortiz, Perroni and Pérez-Elizalde (2018) established that natural tree systems (Vachellia pennatula (Schltdl. & Cham.) Seigler & Ebinger and Lysiloma acapulcense (Kunth) Benth.), and pastures (M. maximus and Hyparrhenia rufa (Nees) Stapf) increase the contents of organic carbon, organic matter, ammonium, and total phosphorus, through mechanisms such as nitrogen fixation, and nitrogen and phosphorus sequestration by microbial activity, and through litterfall and decomposition.

These increases in protein may also be associated with physiological and biochemical adaptations evidenced in shaded grasses. In this regard, Penton and Blanco (1997) affirm that, under shade conditions, an accumulation of nitrates can occur in the absence of carbohydrates necessary for their reduction to ammonia. This accumulation of nitrates eventually leads to an increase in the percentage share of the protein (N x 6.25) in the dry matter. Similarly, Dias-Filho (2002) indicates that C4 grass species can significantly increase the total concentration of chlorophyll under shade, compared with the same grass under full sun exposure. This increase in chlorophyll is due to the possibility of arranging nitrogen for the production of molecules and proteins linked to photosynthetic pigments (^{Valadares & Niinemets, 2008}), in order to improve efficiency in photosynthesis.

The structural changes evidenced in plant height, leaf width and the LSR values influenced by the silvopastoral arrangements in M. maximus, can be related to the morphological and adaptive plasticity of the grass, and to environmental micro-changes (greater light income) generated by the system when passing from the rainy period to the dry period. In this transition, the trees (for fruit and timber production) experience a total (P. quinata and P. saman) or partial (C. grandis and G. ulmifolia) defoliation phenomena as a defense mechanism against the decrease in rainfall (^{Olivero-Lora, 2011}, ^{Rusch et al., 2014}). The higher light income, as a result of the loss of leaves in some fruit and timber trees during the dry period, could stimulate the morphological plasticity of M. maximus, which resulted in a higher increase in the average height of the plant and width of the leaves in the p-Arbor, p-Arbust-Arbor and p-Arbust-Arbor-M arrangements.

The elongation of the stems in grasses under shade conditions is considered an adaptive mechanism that seeks to increase their competitive capacity and improve the distribution of light along the canopy (^{Guenni et al., 2008}); similarly, the width of the leaf reflects an adaptive response of plant species subjected to stress conditions (^{Baruch et al., 2017}; ^{Guerin et al., 2012}). Paciullo et al. (2017) recorded stem elongation rates of 0.06 to 0.19 mm/day in M. maximus from 0 to 58 % light interception. Medinilla et al. (2013) reported increases of 12 % in plant height for M. maximus under the shade of G. sepium, compared to growth under full sun exposure. Regarding leaf width, Gómez, Navarro and Pérez (2016) indicated that under the shade of P. saman, M. maximus registered a significant increase of 0.3 cm, compared with the grass under full sun exposure.

Conclusions

Silvopastoral systems with tree cover generated an adaptive response in M. maximus in variables such as crude protein content, plant height, leaf width, and the leaf: stem ratio. Results showed that the grass was adapted to the light reduction conditions in the sps, which is promising in the management of grazing, with possible benefits in the contribution of forage with higher protein quality to the diet of grazing animals.

Disclaimer

This research was developed within the framework of the project "Comprehensive Assessment of the Benefits of Multiple Strata Silvopastoral Systems on Soil Sustainability and Animal Productivity in the Dual Purpose System of the Caribbean Region of Colombia", funded by Ministerio de Agricultura y Desarrollo Rural (madr) [2010 Research Call] and executed by AGROSAVIA (formerly Corpoica).