Does macauba cake alter nutrient digestibility and microorganism population in the rumen of sheep?

doi:10.21203/rs.3.rs-2484914/v1

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Does macauba cake alter nutrient digestibility and microorganism population in the rumen of sheep?

https://doi.org/10.21203/rs.3.rs-2484914/v1

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published 09 Jun, 2023

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This study aimed to determine the effects of including macauba cake (MC) in the diets of Santa Ines sheep on nutrients digestibility, and the population of microorganism in the rumen (total bacteria, anaerobic fungi, methanogenic organisms, Ruminococcus flavefaciens, and Fibrobacter succinogenes). Twenty male sheep were distributed in a randomized block design with four MC treatment diets (0, 10, 20, and 30% of total dry matter). MC inclusion did not affect the dry matter, organic matter, or crude protein intake, but increased the ether extract, neutral detergent fiber, and acid detergent fiber intake, mainly because of changes in the concentrations of these components in diets with a higher level of MC. With MC inclusion, a linear decreasing effect was observed for the dry matter and organic matter digestibility, and a quadratic effect with a maximum point of 21.5% was observed for the acid detergent fiber digestibility. MC inclusion reduced anaerobic fungal populations and increased methanogenic populations. The increase in methanogenic organisms can be associated with the higher fiber content in diets containing MC. The inclusion of macauba cake in the diet of lambs reduced the dry matter digestibility, promoted an antifungal effect and increased the methanogenic population.

Acrocomia aculeata

by-product

lamb

methanogenic organisms

The use of agro-industrial residues in ruminant feed has increased due to the greater availability of these by-products (Santos et al. 2015), the possibility for reducing feeding costs by replacing traditional foods (Oliveira et al. 2012), and the reduced environmental effects because most of the by-products are environmental waste management problems.

The macauba (Acrocomia aculeata (Jacq.) Lodd. Ex Mart.) is a highly productive oil seed palm, which is native to South America. It has attracted interest as an oil source, with potential for the production of biodiesel, cosmetics, and food. The oil from the fruit pulp has high levels of palmitic (C16:0), oleic (C18:1), and linoleic (C18:2) acids, which account for approximately 90% of total fatty acids (Coimbra and Jorge 2012).

During the process of oil extraction using a hydraulic press, large quantities of biomass residue are generated, which represent 50% of the total quantity of the processed fruit. This residual biomass, called macauba cake (MC), contains low levels of protein (7.41 ± 0.75) and high levels of fiber (67.03 ± 4.85) and ether extracts (17.34 ± 2.30) (Azevedo et al. 2013, Rufino et al. 2011, Santos et al. 2017). Therefore, MC can be considered an alternative ruminant feed. However, a high lipid level in the diet of ruminants (more than 5% of fatty acids in the dietary DM) can inhibit rumen fermentation, Gram-positive bacteria, Archaea, and protozoa (Palmquist and Jenkins 1980).

A recent study demonstrated that 100 g kg^-1 of MC in diet reduced ruminal protozoa concentrations in dairy cows (Santos, Magalhães, Azevedo, Vieira, França, Geraseev and Duarte 2015) and Santa Ines lambs (Santos, Azevedo, Júnior, Rodriguez, Duarte and Geraseev 2017). This alteration in ruminal protozoa suggests that other ruminal populations, such as cellulolytic bacteria, could also be affected, which would change the bioavailability of nutrients. The high lipid and fiber contents in MC may decrease animal intake and affect digestibility and performance due to an interference with fiber digestion. In this study, the aims were to evaluate the digestibility of nutrients, and the changes in some ruminal microorganism populations in sheep fed diets containing different amounts of macauba cake.

Twenty castrated male Santa Ines lambs were used. Initially, the animals were individually identified, treated for ecto- and endo-parasites, and immunized for clostridiosis. The sheep were housed in metabolic cages (1.10 × 1.10 m), which had individual feeders, waterers, and collectors of feces and urine.

The animals were divided into four groups using a randomized block design to evaluate the effects of different MC levels in the diet (0, 10, 20, and 30% of DM). The blocks were defined according to the initial body weight: the mean live weights of the first fifth blocks were 52.17 ± 4.8 kg, 48.17 ± 1.25 kg, 45.62 ± 2.1 kg, 37.65 ± 6.1 kg, and 32.75 ± 6.3 kg, respectively.

The diets were prepared according to the recommendations of the (NRC,2007) for metabolizable energy requirements, and consumption was regulated to maintain 10% of leftovers (Table 1). The diet was provided twice a day at 07:00 and 15:00. For each block, the experimental period consisted of 15 d of adaptation and 5 d of sample collection. The experimental collection period included the measurements of the total amount of leftovers and daily production of feces per animal. Representative samples of the leftovers, feces and urine were collected daily. To avoid the loss of nitrogenous compounds by volatilization, 100 mL of 10% sulfuric acid (H₂SO₄) was added to the urine collectors. The samples were frozen at -20 ℃ for subsequent laboratory analyses.

Table 1

Ingredients and chemical composition (g/kg DM) of experimental diets
	Macauba cake inclusion (%)
	0	10	20	30
Ingredients (g/kg DM)
Sorghum Silage	500.0	500.0	500.0	500.0
Soybean meal	54.9	64.2	73.5	82.9
Ground corn	377.4	268.8	160.2	51.6
Cotton cake	5.00	5.00	5.00	5.00
Macauba cake	0	100.00	200.00	300.00
Mineral mixture(¹⁾	6.5	5.4	4.3	3.2
Salt	5.0	5.0	5.0	5.0
Bicalcium phosphate	6.2	6.5	6.9	7.3
Chemical composition (g/kg DM)
Dry Matter (g/kg as fed)	604.8	609.6	614.4	619.4
Ash	78.1	48.2	51.5	54.8
Crude protein	123.0	122.9	122.9	123.0
Neutral detergent fiber	429.1	468.7	508.2	547.8
Acid detergent fiber	213.4	249.6	285.8	322.0
Ether extract	49.5	59.0	68.6	78.2
Non fibrous carbohydrate	320.3	301.2	248.8	196.2
Neutral detergent insoluble nitrogen	12.0	12.6	12.9	11.9
Acid detergent insoluble nitrogen	1.6	1.7	1.6	1.8
⁽¹⁾Guaranted level: 130–150 g calcium, 65 g phosphorus, 130 g sodium, 12 g sulfur,10 g magnesium, 1000 mg iron, 3000mgmanganese, 80mg cobalt, 5000mg zinc, 60 mg iodine, 10 mg selenium, Vitamina A 50000 U. I., Vitamina E 312 U. I.

Ground samples of the diets, leftovers, and feces were analyzed according to the Association of Official Analytical Chemists (AOAC,1998), for DM (method 934.01), ash (method 942.05), crude protein (CP, method 954.01), and ether extract (EE, method 920.39). Neutral detergent fiber (NDF), (Van Soest et al. 1991) and acid detergent fiber (ADF) analyses (AOAC, 1998, method 973.18) were performed using an ANKOM200 Fiber Analyzer unit (ANKOM Technology Corporation, Fairport, New York, USA). Sodium sulfite and alpha amylase were used in the determination of NDF according to INCT-CA (Detmann et al. 2012). Non-fiber carbohydrates were calculated as: NFC = 100 - (% NDF + % EE + % CP + % Ash). The gross energy (GE) of the feed, feces, and urine was determined using an adiabatic calorimeter.

The DM, organic matter (OM), CP, EE, NDF, and ADF intakes were calculated by the difference in the daily weight offered and leftover by lambs. The in vivo digestibility of each chemical component (DM, OM, CP, EE, NDF, ADF) was calculated for each animal using the average individual nutrient intake and fecal output.

Four hours after the feed on the last day of the collection period, the rumen fluid was extracted from each animal using an esophageal probe coupled to a vacuum pump. A single sample per animal was taken, Rumen fluid samples were stored in a freezer at -20 ℃ for subsequent analysis.

Before DNA extraction, the sample was well homogenized with a vortex. DNA extraction was performed according to the method described by Makkar (2005) and was carried out in duplicate. The DNA concentration and purity of the sample (260 nm/280 nm) were determined using a Nanodrop 1000 spectrophotometer at absorbances of 260 and 280 nm. The extracted DNA was used as a template for the quantitative PCR assay using primer pairs for rumen bacteria, rumen fungi, Ruminococcus flavefaciens, Fibrobacter succinogenes, and rumen methanogens, as described by Denman and McSweeney (2006) and Denman et al. (2007). The DNA samples were diluted to a final concentration of 10 ng/µL. The primers were used at a concentration of 10 mM along with SYBR Green. The final volume of the reaction was 25 µL.

DNA amplification was performed on an Applied Biosystems 7500 thermal cycler using the following program: 1 cycle of 95 ℃ for 5 min; 40 cycles of 95 ℃ for 10 s and 60 ℃ for 30 s; and one cycle of 95 ℃ for 2 min, 60 ℃ for 15 s, and 95 ℃ for 15 s. The microbial population levels were expressed relative to the total bacterial population (ΔCt). These ΔCt values were calculated by the difference between the cycle threshold (Ct) values of the target and reference genes (16S rRNA of the bacteria). The ΔΔCts were determined by the difference between the ΔΔCts of the target groups in the experimental and control diets. The percentages of rumen fungi, Ruminococcus flavefaciens, Fibrobacter succinogenes, and rumen methanogens relative to the total bacterial population were calculated from the ΔCt values as 100 × (2^∆Ct)^-1 (Denman and McSweeney 2006) and the expression of the target groups relative to the control treatment as 2^−Δ∆Ct.

The data concerning the nutrient intake and digestibility were analyzed using PROC REG, part of the statistical software Statistical Analysis System (SAS, 2004). For microorganisms, the variance analyses were performed using the AOV function and Duncan’s test in the ExpDes package. In the multivariate analysis, the original data were standardized, and the principal components were obtained using the princomp function of R software.

Including MC in the diet of the sheep did not change the intake of DM, OM, or CP (Table 2). However, MC inclusion increased the intake of EE, NDF, and ADF (P < 0.01), mainly because of changes in the concentrations of these components in diets with elevated MC levels (Table 1). Inclusion of MC reduced the in vivo digestibility of DM and OM, but increased the digestibility of ADF (P < 0.01), with a peak at the 21.5% MC inclusion level (Table 2). The lower DM and OM digestibility with MC inclusion was due to the increase in the fibrous fraction, which is common when there is a substitution of conventional for alternative ingredients. However, no effect was observed in CPD, EED and NDFD.

Table 2

– Digestibility and nutrients intake of lambs fed different levels of macauba cake
	Macauba cake inclusion (%)					P value
	0		10	20	30	Linear		Quadratic
DMI (g LW^0.75day⁻¹)	58.0	53.6		56.5	56.1	0.816		0.138
OMI (g LW^0.75day⁻¹)	55.4	51.0		52.5	53.0	0.422		0.089
CPI (g LW^0.75day⁻¹)	6.79	6.84		7.02	7.12	0.1550		0.3719
EEI (g LW^0.75day⁻¹)⁽¹⁾	3.43	4.36		5.26	6.08	< 0.01		< 0.01
NDFI (g LW^0.75day⁻¹)⁽²⁾	24.9	24.5		28.5	31.6	< 0.01		< 0.01
ADFI (g LW^0.75day⁻¹)⁽³⁾	12.25	13.98		16.28	18.81	< 0.01		< 0.01
DEI (kcal day^− 1)	148.77	141.34		147.42	143.04	0.5040		0.7767
DMD (%)⁽⁴⁾	66.98	65.45		64.73	58.54	< 0.01		< 0.01
OMD (%)⁽⁵⁾	69.70	67.47		65.91	59.52		< 0.01	< 0.01
CPD (%)	67.98	63.19		66.93	61.70	0.0534		0.1574
EED (%)	86.65	89.32		91.90	90.34	0.1885		0.2787
NDFD (%)	55.51	59.21		59.26	56.80	0.7286		0.5215
ADFD (%)⁽⁶⁾	50.38	55.38		59.15	57.02	< 0.01		< 0.01
Dry matter intake (DMI), organic matter intake (OMI), crude protein intake (CPI), ethereal extract intake (EEI ), neutral detergent fiber intake (NDFI), acid detergent fiber intake (ADFI),digestible energy intake (DEI), dry matter digestibility (DMD), organic matter digestibility (OMD), crude protein digestibility (CPD), ethereal extract digestibility (EED), neutral detergent fiber digestibility (NDFD) and acid detergent fiber digestibility (ADFD).
⁽¹⁾y quadratic = 3.4275 + 0.0967X -0.0003X²; R² = 88.91%; ⁽²⁾y quadratic = 24.62 -0.0169x + 0.0086x²; R² = 91.70%;⁽³⁾y quadratic = 12.233 + 0.1598X + 0.002 X²; R² = 92.30%; ⁽⁴⁾y quadratic = 66.59 -0.0928X-0.0118X²; R² = 50.36%; ⁽⁵⁾y quadratic = 69.425 -0.009X – 0.0104X²; R² = 74.54%; ⁽⁶⁾y quadratic = 50.179 + 0.781X – 0.01819X²; R² = 48.40%.

The MC inclusion in sheep diets did not affect Ruminococcus flavefaciens and Fibrobacter succinogenes relative quantification (%), however it significantly decreased (P < 0.01) the percentage of Anaerobic Fungi at 10% of MC inclusion (Table 3). On the other hand, an increase in the Methanogenic Archaea percentages was only observed at higher inclusion (Table 3).

Table 3

Relative quantification (%) of genes from rumen microbial community expressed as proportion of genes from total bacteria in relation to the experimental diets.
Relative quantification (%)	Macauba cake inclusion (%)				P value
	0	10	20	30	Linear	Quadratic
Anaerobic Fungi⁽¹⁾	0.241	0.089	0.065	0.067	0.016	0.003
Methanogenic Archaea⁽²⁾	0.029	0.029	0.020	0.076	0.007	0.005
Ruminococcus flavefaciens	0.008	0.003	0.005	0.003	0.479	0.356
Fibrobacter succinogenes	2.543	1.198	1.571	1.590	0.282	0.192
⁽¹⁾ y = 0.2359-0.017x + 0.0004x², R² = 97.56%;⁽²⁾ y = 0.0327-0.0029x + 0.0014x², R² = 85.81%

Principal component analysis (Fig. 1) revealed that the first two components collectively accounted for 90.93% of the variation. In corroboration to our findings, it showed that without MC inclusion in the diet the F. succinogenes, R. flavefaciens, and anaerobic fungal populations, as well as the DM and CP digestibility tended to increase. In addition, at the 30% MC inclusion level, the methanogenic Archaea population, NDF digestibility, ADF digestibility, and EE digestibility showed a tendency to increase.

In this study, the NDF content increased with MC inclusion, however this was not a limiting factor for DM consumption (Table 2). This could be due to the physical processing of the MC, which was ground to a granulometry similar to that of the other foods used in the concentrate, which could reduce the physical effectiveness of the fibrous fraction. Dantas Filho et al. (2007) evaluated the performance of Santa Ines sheep fed diets with different inclusion levels of dehydrated cashew pulp, with NDF levels similar to those in the present study. These authors did not observe differences in the DM intake, although the inclusion of the byproduct increased fiber levels, according to the authors, this fact can be attributed, in part, to the processing of the byproduct, which was finely ground, resulting in a faster rate of passage of the food through the rumen.

Diets composed of high levels of fatty acids, mainly unsaturated, may inhibit the digestion of fiber in the rumen because of their cytotoxicity for microorganisms (Allen 2000). In this study, although there was an increase in the EE level in the diets with MC inclusion, no difference was observed in the NDF digestibility. This was unexpected, as it has been reported in the literature (Santos, Azevedo, Júnior, Rodriguez, Duarte and Geraseev 2017) that MC is substantially composed of unsaturated fatty acids. The percentage of F. succinogenes and R. flavefaciens relative to the total bacterial population was not influenced by the inclusion of MC (Table 3). This may have contributed to the similarity in NDF digestibility

A number of studies have shown that an increase in the EE concentration in the diet reduces the populations of cellulolytic bacteria (Potu et al. 2011), F. succinogenes (Yang et al. 2009), and R. flavefaciens (Wang et al. 2018). Although there was an increase in the dietary EE with MC inclusion, there was also an increase in the NDF content of the diet, which may have contributed to the maintenance of these fibrolytic bacteria. It is important to note that, for all treatments, F. succinogenes comprised a greater percentage of the total bacterial population than R. flavefaciens. This was unsurprising as F. succinogenes has been described as one of the major cellulolytic bacterial species present in the rumen (Forsberg et al. 1997).

The increase in Archaea (Table 3) occurred due to a reduction in the non-fibrous carbohydrate content and an increase in the fibrous fraction in the diet with MC inclusion. Martin et al. (2010) reported a decrease in the ruminal production of CH₄ with diets containing more soluble sugars because of a shift in the VFA production from acetate to propionate. Ruminal dissolved hydrogen positively correlates with total VFA and molar proportions of propionate, and negatively correlates with the molar proportion of acetate and gaseous methane emissions (Wang et al. 2016). In this study, the NDF intake increased with MC inclusion, which may have contributed to the reduction in the ruminal dissolved hydrogen concentration and the increase in methanogenic Archaea.

In this study, we observed a significant reduction in the anaerobic fungal population with MC inclusion (Table 3). The high lipid content potentially reduced the fiber adhesion of zoosporangia and mycelia structures, resulting in the reduced growth of these important fibrolytic microorganisms. Other studies have also reported a reduction in anaerobic fungi with diets containing high levels of lipids. Adult Merino wethers were offered diets containing 15% unprotected and protected cottonseed kernel supplements. Rumen anaerobic fungi were undetectable with 5.9% free lipids, but were present at normal levels with 4 and 2.1% free lipids. Concomitant with the absence of anaerobic fungi, the numbers of protozoa tended to be lower, while the bacterial counts increased (Faichney et al. 2002). Veneman et al. (2015) also reported a reduction in anaerobic fungi with the inclusion of linseed oil in the diet of dairy cows.

In a previous study, we evaluated the rumen protozoa profile of lambs fed diets with MC. The concentrations of small, medium, and large protozoa, as well as the total, were maximal at an inclusion of 10% in the diet. Above this level, theses ciliate populations substantially decreased along with a reduction in the genus diversity. The fatty acid composition of the MC (per kg fatty acids) was: 15.3 g of C12:0, 14.7 g of C14:0, 178.0 g of C16:0, 40.6 g of C16:1, 18.0 g of C18:0, 550.3 g of C18:1, 150.0 g of C18:2, 17.6 g of C18:3, and 15.5 g of other acids. A ratio of 1.0/3.4 saturated/unsaturated fatty acids was associated with antiprotozoal effects (Santos, Azevedo, Júnior, Rodriguez, Duarte and Geraseev 2017). The mix of fatty acids might also promote the antifungal effect observed in the present study, which requires elucidation in future studies.

Agricultural residues, like MC, are lower cost alternatives to be used in ruminant diets. Our study revealed that increasing level of this residue (up to 30% of total DM) reduced dry matter digestibility, promoted an antifungal effect, and increased the methanogenic population. This could be explained by the increase of NDF and EE contents of those diets, however further studies are necessary to fully understand how microbial colonization occurs and its effect on animal performance.

Funding

This project was financed by National Council for Scientific and Technological Development - CNPq (475368 / 2012-6), Coordination of Superior Level Staff Improvement - CAPES (code 001) and the Pro-Reitoria de Pesquisa of Federal University of Minas Gerais - PRPq/UFMG

Conflict of Interest Statement

The author declares that there are no conflicts of interest.

Author Contributions

Luciana Castro Geraseev, Eduardo Robson Duarte and Niurca González Ibarra conceived and designed the research. Edvaldo Alves Vieira, Niurca González Ibarra and Sarah Silva Santos conducted experiment. Alcinei Mistico Azevedo, Amália Saturnino Chaves, Niurca Gonzáles Ibarra, Eduardo Robson Duarte and Luciana Castro Geraseev analyzed the data. The first draft of the manuscript was written by Edvaldo Alves Vieira, Eduardo Robson Duarte, Rodrigo Augusto Cortêz Passetti, Niurca González Ibarra and Luciana Castro Geraseev. All authors read and approved the final manuscript.

Data Availability Statements

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Ethics approval

The animal experiments were conducted in accordance with the ethical principles of animal experimentation, approved in protocol 267/2013 by the committee of ethics in animal experimentation at the Federal University of Minas Gerais.

Acknowledgements

We would like to thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (Fapemig), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior of the Brazil (CAPES), and the Pro-Reitoria de Pesquisa of the Universidade Federal de Minas Gerais for the financial support of this study.

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Does macauba cake alter nutrient digestibility and microorganism population in the rumen of sheep?

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