The impact of reducing dietary crude protein and increasing total dietary fiber on hindgut fermentation, the methanogen community and gas emission in growing pigs

doi:10.1016/j.anifeedsci.2018.09.005

Animal Feed Science and Technology

Volume 245, November 2018, Pages 54-66

https://doi.org/10.1016/j.anifeedsci.2018.09.005 Get rights and content

Highlights

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Despite the enteric origin, a fraction of 9.7% of CH₄ emitted from the slurry pit.
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Methanogen concentration increased throughout the cecum-colon tract.
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NH₃ losses reduced 8.6% per each percentage decrease in CP content of the diet.
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Differences in CH₄ emission did not reflect the methanogen concentration.

Abstract

Sixty-four cross bred 6 week-old intact male pigs (initial BW = 13.8 ± 2.3 kg) were randomly distributed to 4 separated modules using a three-phase feeding program in which two dietary crude protein (CP) and total dietary fiber (TDF) levels were tested in a 2 × 2 factorial arrangement under a commercial-like production system. The room air was sampled and analyzed for NH₃ and CH₄ while the slurry pit air was sampled and analyzed for CH₄ content during the early growing (phase I, 13.8–38.6 kg of body-weight), growing (phase II, 38.6–72.8 kg of body-weight) and finishing periods (phase III, 72.8–108.7 kg of body-weight); at the end of the finishing phase, 16 random pigs were sacrificed and cecum and colon contents were sampled to determine fermentation and microbial parameters. The pH and ammonium content increased with digesta transit being lower in cecum (6.0 and 69.7 mg/L) than in colon (6.3 and 156.3 mg/L) whereas the opposite trend was seen for total VFA and acetate (175.2 mM and 62.6 mol/100 mol vs. 141.1 mM and 57.2 mol/100 mol, respectively; P < 0.05). Low protein (LP) and high fiber (HF) diets showed a higher NH₃ concentration in the colon but not in cecum samples. Dietary fiber also altered intestinal VFA concentration where animals fed Low fiber (LF) diet showed high VFA’s concentrations and such effect was more pronounced in colon samples. Total NH₃ (1.8, 4.8 and 8.5 g/day) and methane (2.5, 3.5 and 7.5 g/day for Phase I, II and III, respectively) emissions increased consistently with age (P < 0.05), dietary CP level increased NH₃ volatilization (6.3 vs. 3.8 g/d for high protein (HP) and LP diets respectively; P < 0.01) and fiber tended to increase methane emission (5.0 vs. 4.0 for HF and LF diets, respectively P < 0.1). The methane production measured at slurry pit contributed significantly to total CH₄ emission (3.26, 9.02 and 16.91% in the phases I, II and III respectively). Dietary CP increased total bacteria (TB; 9.7 vs. 9.5; P < 0.03) and total methanogenic archaea (TMA; 7.2 vs. 6.4; P < 0.01) abundances in the intestinal as well as the slurry (6.8 vs. 6.3 Log n° copy/ g fresh matter (FM); P < 0.01) samples whereas TDF did not alter microbial titers. Differences in CH₄ emission did not reflect the TMA concentration in hindgut contents.

Introduction

The environmental impact of the intensified pig production in Europe is significant. Pig manure is a source of greenhouse gases (GHG) like methane (CH₄) and other harmful gases such as ammonia (NH₃). Increased public concern on the livestock environmental footprint made EU legislation to regulate the potential quota of atmospheric pollution (IPPC Directive; Directive EU 2016/2284 on the reduction of national emissions of certain atmospheric pollutants) where animal nutrition is considered as a key strategy. Under intensive production, ≈ 20% dietary N is retained in the animal’s body (Canh et al., 1997). Irreversible NH₃-losses (through the urine and feces) may approach 50% of N intake (Ryden et al., 1987; Hartung and Phillips, 1994) due to the excess or unbalanced dietary protein together with manure-handling strategies. Methane is identified as a main contributor to global warming (Johnson et al., 2002) and represents an irreversible energy loss. Methane production in pigs has been commonly linked to dietary gross energy intake (1.2% of DE intake; Christensen, 1987), and a positive correlation between fiber intake and methanogens diversity (Cao et al., 2012) or abundance (Liu et al., 2012) has been reported. Methanogens have been identified in hindgut digesta and pig feces, being the genus Methanobrevibacter (Steinberg and Regan, 2009; Luo et al., 2012) the most abundant. CH₄ production is the main disposal sink for reducing equivalents (H²), and a competition between H²-consuming organisms (hydrogenotrophic) and sulphate reducing bacteria (SRB) has been reported in the human colon (Bernalier et al., 1996) and rabbit caecum (Belenguer et al., 2011) but factors that determine the end-routes of reducing equivalents (H²) are not well understood.

This study was designed to determine the impact of dietary factors on emissions of harmful gases in pigs under commercial-like conditions and to analyze the ecology of lower gut methanogens to prevent the negative impact of CH₄ production on energy utilization and the environment.

Section snippets

Materials and methods

All procedures were carried out under Project License CEEA 03/01-10 and approved by the in-house Ethics Committee for Animal Experiments at the University of Lleida. The care and use of animals were in accordance with the Spanish Policy for Animal Protection RD 53/2013, which meets the European Union Directive 2010/63 on the protection of animals used for experimental purposes.

Results

The experiment was carried out using a three phase feeding system, in which the amino acid supply was adjusted for each production stage to match nutrient intake with requirements. Intake, digestibility, growth and carcass characteristics were fully addressed and discussed previously in Morazán et al. (2015a).

Experimental approach

In the present approach CH₄ emission and NH₃ volatilization were analyzed simultaneously in an open-circuit system while trying to maintain the “standard” commercial housing conditions and minimizing the impacts of the experimental handling over the animals.

Total emissions included gases originating from the digestive tract and also those originated from the slurry storage; in this sense, authors are aware of a wide variation existing in both housing conditions (i.e. aeration level,

Conclusions

In the present approach, in an open-circuit system designed to maintain commercial-like conditions NH₃-volatilization increased with dietary CP supply and growth phase and proportionally reduced as a whole, a mean values of 8.6% per each percentage unit (%) of CP reduction. Enteric origin constituted the main source for CH₄ emission, although a relevant fraction (averaging 9.7%) did come from the slurry pit. Pigs of HF diets trended to increase CH₄ emission. Methanogen concentration increased

Declarations of interest

None.

Acknowledgments

This work is part of the Feed-a-Gene project and was supported by the European Union's H2020 program under National Institutes of Health [grant number 633531, 2016]. Authors would like to thank Dr. David Parker who generously gave his assistance and constructive comments to the manuscript, his effort is sincerely appreciated.

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The impact of reducing dietary crude protein and increasing total dietary fiber on hindgut fermentation, the methanogen community and gas emission in growing pigs

Highlights

Abstract

Introduction

Section snippets

Materials and methods

Results

Experimental approach

Conclusions

Declarations of interest

Acknowledgments

Livest. Sci.

Anim. Feed Sci. Tech.

FEMS Microbiol. Ecol.

Livest. Prod. Sci.

Livest. Sci.

Livest. Prod. Sci.

Anim. Feed Sci. Tech.

Agric. Ecosyst. Environ.

Livest. Sci.

J. Agric. Eng. Res.

Agric. Ecosyst. Environ.

Anim. Feed Sci. Tech.

Anim. Feed Sci. Tech.

J. Dairy Sci.

Livest. Sci.

Livest. Sci.

FEMS Microbiol. Ecol.

Methods

FEMS Immunol. Med. Microbiol.

Sci. Total Environ.

Livest. Prod. Sci.

Anim. Feed Sci. Tech.

Anim. Feed Sci. Tech.

Livest. Sci.

Environ. Pollut.

Anim. Feed Sci. Tech.

Trends Microbiol.

J. Dairy Sci.

Divergence and Redundancy of 16S rRNA Sequences in Genomes with Multiple rrn Operons

J. Bacteriol.

Field Performance Measurement of Fan Systems

Official Methods of Analysis

Methanogenesis in rabbit caecum as affected by the fermentation pattern: in vitro and in vivo measurements

World Rabbit Sci.

Enumeration of selected anaerobic bacterial groups in cecal and colonic contents of growing-finishing pigs

Appl. Environ. Microbiol.

Influence of dietary factors on nitrogen partitioning and composition of urine and feces of fattening pigs

J. Anim. Sci.

Diversity of methanogens in the hindgut of grower and finisher pigs

Afr. J. Biotechnol.

Effect of dietary fiber on the methanogen community in the hindgut of Lantang gilts

Animal