Chicory as potential fibre source for pigs and poultry

Background

Currently, the inclusion of forage in diets for pigs and poultry is limited. However, a number of beneficial effects on animal health and welfare have been found, and presumable the inclusion of fibre in diets for mono-gastric animals will increase in the future. Chicory (Cichorium intybus L) is a perennial herb that grows wild in southern Sweden. It has agronomic traits that make it a good complement to other forage plants and inclusion in a seed mix will contribute to a more sustainable and stable ley. The vegetative part of chicory contains around 40 % dietary fibre, of which a significant part is uronic acid. Apart from the vegetative part, the chicory root also has beneficial traits. The root naturally contains 15-20 % inulin and 8-12 % oligofructos, both of which are classified as prebiotics. Prebiotics stimulates the growth of host-beneficial gut bacteria, such as lactobacilli and bifidobacteria. Interestingly, uronic acid may also have similar beneficial effects. Enteric diseases are major problems in piglet and broiler production that negatively affects performance and animal welfare, and cause economic losses for the producers. Therefore, optimising gut health is very important. This can be achieved by increasing the guts own defence mechanisms as this will increase the resistance to enteric diseases. Fibre has been shown to positively affect the gut health by stimulating the gut microflora and the gut immunity. The goal is to find a fibre source that beneficially affect gut health and thereby also exert a positive effect on animal production.

The project

In order to evaluate the potential of chicory (C. intybus L.) as forage crop in organic food production a trans-disciplinary project involving the Departments Animal Nutrition and Management, Crop Production Ecology and Microbiology at SLU has been performed with the financial support of Formas. The project aimed at testing hypotheses about resource utilisation in the field of ley crops containing three complementary functional types of plant species (including C. intybus), nutritional properties of chicory forage for mono-gastric animals and the impact of chicory forage on the gut microbial ecosystem.

Materials and methods

A field experiment consisting of 48 communities was performed to evaluate ecosystem processes in a multi-species mixture with forage species having complementary traits both above- and belowground, and to test hypotheses about resource use (light, N, water) in the communities established and to determine their resistance towards invasion by unsown species. In the experimental setup 30 communities followed a simplex design with 4 pure stands of P. pratense, L. perenne, T. pratense and C. intybus, and 11 mixtures of these 4 species all sown at two densities. The 11 mixtures consisted of four mixtures dominated in turn by each species, six mixtures dominated in turn by pairs of species and the centroid community. The other 18 communities followed a simplex design using M. sativa instead of C. intybus, i.e., four pure stands of P. pratense, L. perenne, T. pratense and M. sativa, and five mixtures of these four species, all sown at two densities.

Three experiments with pigs and one with broiler chickens were performed to evaluate the impact of chicory inclusion on digestibility, growth performance, gut environment, gut development and microbial ecology. In these experiments, chicory forage (40-160 g/kg) and root (60-80 g/kg) alone or in combination was included in cereal-based diets. The gut microbiota was characterized using modern molecular methods (terminal restriction fragment length polymorphism and 454 pyrosequencing) and specific bacterial groups were quantified using culture dependent approaches.

Results and discussion

Species diversity had a positive effect on biomass yield, and the inclusion of a deep-rooted forb in the plant community resulted in a more even yield over the season. N content in the biomass and light availability were not correlated to plant δ13C signatures. Increasing proportions of the deep-rooting species led to depleted δ13C signatures in all species in a community, suggesting alleviation of water stress. Both legumes showed high rates of N fixation. Nitrogen was transferred from both legume species to the two grass species, with more N coming from red clover than from lucerne. In total, 20-30% of the N in the grasses was transferred from the legumes during the two harvest years. Little N transfer took place from red clover to chicory, indicating complementarity in soil N use between the non-legume species. The grasses are either faster in their uptake of soil mineral N, forcing the deep-rooted forb chicory to utilise deeper soil layers, or it could be that the grasses, and not chicory, utilised soil layers with available mineralized biologically fixed N. Functional complementarity and light availability influences the identity and numbers of invading species, and resource availability above- and, particularly below-ground, governs invader performance in terms of biomass production.

Animals retained good performance and health throughout the experiments for all levels of chicory inclusion. In pigs, chicory inclusion did not affect feed intake, weight gain or feed conversion ratio, while a reduction in performance was seen in chickens at high inclusion levels. The total tract digestibility (TTD) of energy, organic matter and crude protein did not differ between the cereal-based basal diet and low inclusion of chicory whereas the TTD was impaired at the highest inclusion level. The TTD of non-starch polysaccharides and especially the uronic acid differed significantly from the cereal-based basal diet and were increased with higher level of chicory inclusion. The gut environment was affected by chicory inclusion with changes in physiology, fermentation pattern and the gut microbiota. The highest inclusion of chicory forage resulted in thinner muscle layer in colon in pigs and thinner caecal mucosa layer in chickens, whereas inclusion of chicory root was associated with increased villus height in pigs. Gut fermentation pattern was influenced by diet type with higher concentrations of lactic acid in ileum of pigs fed chicory roots than in pigs fed the basal diet. In colon, the acetic acid concentration was higher in pigs fed chicory forage than in pigs fed the cereal-based basal diet and diets with chicory root inclusion. The opposite pattern was seen for n-valeric acid with higher concentration for diets including chicory root than in the diets including chicory forage.

Weaned pigs showed large individual variation, however, the faecal microbiota was dominated by members of the same main phyla, namely the Firmicutes (F) and Bacteroidetes (B). The microbiota was dominated by the Lachnospiraceae (F), Ruminococcaceae (F), Lactobacillaceae (F), Streptococcaceae (F) and Prevotellaceae (B) families, but many of the sequences found could not be matched to sequences in public databases indicating novel unrecognized species. Comparing samples at weaning and five weeks post weaning revealed a maturation of the gut microbiota with dramatic changes in the relative abundance of certain genera. Lactobacilli and enterobacteria were less abundant in older pigs whereas the genera Streptococcus, Treponema, Clostridium and Coprococcus were more abundant in older pigs. Despite temporal variation over time, changes in the microbiota could be linked to inclusion of chicory. Microbiota in faecal and digesta samples clustered perfectly according to gut segment with higher bacterial diversity in colon than in ileum but with no correlation to diet type. Terminal ileum was dominated by lactic acid bacteria (LAB) and they were stimulated by the highest inclusion of chicory forage and the diet with both chicory forage and root. LAB, are considered as beneficial bacteria, commonly present as a natural ingredient in fermented products and used in pro-biotic products. In colon, certain butyrate-producing bacteria were positively correlated with inclusion of chicory forage. Butyrate has beneficial effects on health, associated with anti-inflammatory properties, and is used as fuel by the colonic epithelium. Chicory forage diets were correlated with different species of Prevotella. This genus is abundant in the pig gut, but its functional role is not well understood. Inclusion of chicory root was associated with higher abundance of Megasphaera elsdenii in faeces and colon. Interestingly, this bacterium has been reported to play a role for inhibition of the pathogenic bacteria Brachyspira hyodysenteriae. Coliform counts were lower and the lactobacilli:coliform ratio was higher in the diet that included both chicory forage and root than in the basal diet.

Conclusion:

Diverse communities including chicory captured more resources above- and below-ground, and the number of invading species and their biomass production were smaller in mixed than in monoculture plots. Despite high fibre content, the unique properties of chicory forage will allow high inclusion levels in cereal-based in diets for pigs and poultry. Inclusion of chicory forage in cereal-based diets will modulate the gut microbial ecosystem.

Project manager:

Jan Erik Lindberg

PhD students:

Emma Ivarsson, Haoyu Liu

Publications

Peer-reviewed publications

Ivarsson E., Frankow-Lindberg B., Andersson K., Lindberg J.E., 2010. Effect of inclusion level of chicory (Cichorium intybus L.) and ribwort (Plantago lanceolata L.) forage in a cereal-based diet on dietary fibre digestibility in weaned piglets of different age. Livestock Science 134, 202-204.

Ivarsson E., Frankow-Lindberg B.E., Andersson H.K. and Lindberg J.E., 2011. Growth performance, digestibility and faecal coliform bacteria in weaned piglets fed a cereal-based diet including either chicory (Cichorium intybus L.) or ribwort (Plantago lanceolata L.) forage. Animal 5:4, 558–564.

Liu H.Y., Ivarsson E., Jönsson L., Holm L., Lundh T. and Lindberg J.E., 2011. Growth performance, digestibility, and gut development of broiler chickens on diets with inclusion of chicory (Cichorium intybus L.). Poultry Science 90, 815-823.

Frankow-Lindberg, B.E., 2012. Grassland plant species diversity decreases invasion by increasing resource use. Oecologia, 169, 793-802.

Ivarsson, E., Liu, H. Y., Dicksved, J., Roos, S. and Lindberg, J. E., 2012. Impact of chicory inclusion in a cereal-based diet on digestibility, organ size and faecal microbiota in growing pigs. Animal 6(7), 1077-1085.

Ivarsson, E., Andersson, R. and Lindberg, J. E., 2012. Molecular weight distribution of soluble fiber fractions and short chain fatty acids in ileal digesta of growing pigs. Journal of Animal Science 90, 65-67.

Ivarsson, E., Andersson, R. and Lindberg, J. E., 2012. Digestibility of fibre sources and molecular weight distribution of fibre fractions in ileal digesta of growing pigs. Archives of Animal Nutrition 66, 445-457.

Liu, H. J., Ivarsson, E., Dicksved, J., Lundh, T. and Lindberg, J. E., 2012. Dietary inclusion of chicory (Cichorium intybus L.) affects pig intestinal micro-environment and gut microbiota. Applied and Environmental Microbiology 78 (12), 4102-4109.

Liu, H. Y., Lundh, T., Dicksved, J. and Lindberg, J. E., 2012. Expression of heat shock protein 27 in gut tissue of growing pigs fed diets without and with inclusion of chicory fiber. Journal of Animal Science 90, 25-27.

Frankow-Lindberg, B.E. and Dahlin A.S., 2013. N2 fixation, N transfer and yield in grassland communities including a deep-rooted legume or non-legume species. Plant and Soil, doi: 10.1007/s11104-013-1650-z (In press).

Manuscripts

Dicksved J., Andersson A.F., Zheng Z., Jansson J.K. and Lindberg J.E. Barcoded pyrotag sequencing of the fecal microbiota of growing pigs fed a cereal based diet including chicory Cichorium intybus L.) or ribwort (Plantago lanceolata L.) forage. Manuscript

Frankow-Lindberg, B.E. and Wrage, N. 2013. Temporal changes of 13C in grassland plant communities of functionally contrasting species composition. Manuscript

Liu, H.Y., Dicksved, J., Lundh, T. and Lindberg, J.E., 2013. Expression of heat shock protein 27 and 72 correlates with specific commensal microbes in different regions of the gastrointestinal tract. Manuscript

Liu, H.Y., Lundh, T., Roos, S., Jonsson, H., Ahl, D., Dicksved, J. and Lindberg, J.E., 2013. Effects of Lactobacillus johnsonii and Lactobacillus reuteri on gut barrier function and heat shock proteins in porcine IPEC-J2 intestinal epithelial cells. Manuscript

Conference publications

Frankow-Lindberg, B.E. and Dahlin, A.S., 2010. Transfer of nitrogen from legumes to non-nitrogen fixing species in multi-species swards. Proceedings of the NJF Seminar 432: The potential of forage legumes to sustain a high agricultural productivity, pp. 83-86.

Frankow-Lindberg, B.E., 2010. Richness of unsown plant species in a sown ley crop. Grassland Science in Europe. Vol. 15: 794-796.

Ivarsson E. and Lindberg J.E., 2010. Nutrient utilization and growth performance in growing pigs fed a cereal-based diet with chicory forage (Cichorium intybus L.) inclusion. 3rd International Symposium on Energy and Protein Metabolism and Nutrition. EAAP Publication 127, 617-618.

Lindberg, J. E. and Frankow-Lindberg, B. E., 2006. The effect of feeding two grassland herbs on the growth performance of weaned piglets. Grassland Science in Europe. Proceedings of the 21st General Meeting of the European Grassland Federation, Badajoz, Spain. Vol. 11, pp. 486-488.

Frankow-Lindberg, B.E., 2010. Richness of unsown plant species in a sown ley crop. Grassland Science in Europe. Vol. 15: 794-796.

Liu H.Y. and Lindberg J.E., 2010. Nutrient utilization and growth performance in broiler chickens fed a cereal-based diet with chicory forage (Cichorium intybus L.) inclusion. 3rd International Symposium on Energy and Protein Metabolism and Nutrition. EAAP Publication 127: 619-620.

Conference abstracts

Dicksved J, Lindberg JE, Haglund AG, Rosenquist M and Jansson JK. 2006. Dietary modulation of the pig intestinal microbiota. 11th International symposium on microbial ecology (ISME), August 2006, Vienna, Austria.

Ivarsson E. and Lindberg J.E., 2010. Impact of feeding diets with inclusion of chicory on the faecal bacteria in growing pigs. 61st Annual meeting of the European association for animal production, Heraklion, Greece, August 23-27, 2010. Book of abstract 16, 49.

Ivarsson E. and Lindberg J.E., 2011. Nutrient utilization of chicory forage (Cichorium intybus L.) in growing pigs. 24th Nordic Feed Science Conference, Uppsala, Sweden June 14-16, 2011. NJF Report 7:3, 179.

Liu HY and Lindberg JE., 2010. Chicory (Cichorium intybus L.) in weaned pig diets: effects on ileum and colon. 61st Annual Meeting of the European Association for Animal Production-Crete (Greece), August, 2010.