Rumen disappearance of tannins from tropical tannin-rich plants: interplay between degradability, methane production and adherent rumen microbiota

Condensed tannins in plants are found free and attached to protein and fibre but it is not known whether these fractions influence degradation and rumen function. The aim of the study was to explore the rumen degradation of tropical tannins-rich plants and elucidate their relationship with the disappearance of condensed tannins fractions. The effects on fermentation parameters and microbial communities colonising plant particles in the rumen was also assessed. We used in situ and in vitro approaches to study four leguminous: leaves from Calliandra calothyrsus, Gliricidia sepium, and Leucaena leucocephala, Acacia nilotica pods and the leaves of two agricultural by-products: Manihot esculenta and Musa spp. Plants were analysed to quantify levels of hydrolysable tannins, free condensed tannins, protein-bound condensed tannins and fibre-bound condensed tannins. Rumen dry matter, nitrogen and fibre (NDF) degradability, rumen disappearance of tannin fractions and microbial colonisation of plants was assessed in situ. The methane-mitigation potential of tannin-rich plants compared to a tropical forage without tannins was assessed in vitro. All plants contained more than 100 g/kg of condensed tannins with a large proportion (32 to 61%) bound to proteins. Calliandra calothyrsus had the highest concentration of condensed tannins at 361 g/kg, whereas Acacia nilotica was particularly rich in hydrolysable tannins (350 g/kg). Hydrolysable and free condensed tannins from all plants completely disappeared after 24 h incubation in the rumen. Disappearance of protein-bound condensed tannins was more variable with Gliricidia sepium showing the highest proportion (93%), Manihot esculenta and Musa spp. showed intermediate values of disappearance, and no disappearance was observed from Calliandra calothyrsus leaves. In contrast, fibre-bound condensed tannins disappearance averaged ∼82% and did not vary between plants. Disappearance of bound fractions of condensed tannins was not associated with degradability of plant fractions. Dry matter and nitrogen degradation were similar for all plants except Calliandra calothyrsus and Musa spp. that showed lower values. Calliandra and Acacia nilotica had also a lower NDF degradation. Methane production was also lower for these plants and for Leucaena leucocephala although for the latter total volatile fatty acids production was not affected and was similar to control. The presence of tannins interfered with the microbial colonisation of plants. Each plant had distinct bacterial and archaeal communities after 3 and 12 h of incubation in the rumen and distinct protozoal communities at 3 h. Adherent communities in tannin-rich plants had a lower relative abundance of fibrolytic microbes, notably Fibrobacter spp. Whereas, archaea diversity was reduced in high tannin-containing Calliandra calothyrsus and Acacia nilotica at 12 h of incubation. Here we show that the total amount of hydrolysable and condensed tannins contained in a plant govern the interaction with rumen microbes affecting degradability and fermentation. The effect of protein- and fibre-bound condensed tannins on degradability is less important.