Decreasing methane yield with increasing food intake keeps daily methane emissions constant in two foregut fermenting marsupials, the western grey kangaroo and red kangaroo

Abstract

Fundamental differences in methane (CH 4 ) production between macropods (kangaroos) and ruminants have been suggested and linked to differences in the composition of the forestomach microbiome. Using six western grey kangaroos (Macropus fuliginosus) and four red kangaroos (Macropus rufus), we measured daily absolute CH 4 production in vivo as well as CH 4 yield (CH 4 per unit of intake of dry matter, gross energy or digestible fibre) by open-circuit respirometry. Two food intake levels were tested using a chopped lucerne hay (alfalfa) diet. Body mass-specific absolute CH 4 production resembled values previously reported in wallabies and non-ruminant herbivores such as horses, and did not differ with food intake level, although there was no concomitant proportionate decrease in fibre digestibility with higher food intake. In contrast, CH 4 yield decreased with increasing intake, and was intermediate between values reported for ruminants and non-ruminant herbivores. These results correspond to those in ruminants and other non-ruminant species where increased intake (and hence a shorter digesta retention in the gut) leads to a lower CH 4 yield. We hypothesize that rather than harbouring a fundamentally different microbiome in their foregut, the microbiome of macropods is in a particular metabolic state more tuned towards growth (i.e. biomass production) rather than CH 4 production. This is due to the short digesta retention time in macropods and the known distinct 'digesta washing' in the gut of macropods, where fluids move faster than particles and hence most likely wash out microbes from the forestomach. Although our data suggest that kangaroos only produce about 27% of the body mass-specific volume of CH 4 of ruminants, it remains to be modelled with species-specific growth rates and production conditions whether or not significantly lower CH 4 amounts are emitted per kg of meat in kangaroo than in beef or mutton production.

Review: Comparative methane production in mammalian herbivores

“…Reports stating that various vertebrate groups do not produce methane (CH 4 ) or do not harbour methanogens were met by opposite evidence. This includes the ostrich (Struthio camelus) (Swart et al, 1993;Miramontes-Carrillo et al, 2008;Matsui et al, 2010), kangaroos (Dellow et al, 1988;Vendl et al, 2015), mammalian carnivores (Hackstein and Van Alen, 1996;Middelbos et al, 2008;Tun et al, 2012), sea cows (Marsh et al, 1978;Goto et al, 2004), colobus monkeys (Bauchop and Martucci, 1968;Ohwaki et al, 1974) and arvicoline rodents (Hackstein and Van Alen, 1996; this study). Table S1 gives an exemplary overview over mammal species in which CH 4 emissions or methanogen presence has been detected.…”

“…Abandoning clear categories of CH 4 -producing digestion types raises the question whether other rules can be gleaned from the comparative dataset. There are well-established relationships between food intake or digesta retention and CH 4 yield in domestic ruminants (Okine et al, 1989;Lassey et al, 1997;Barnett et al, 2012;Hammond et al, 2014;Barnett et al, 2015) and in individual groups of nondomestic species (Frei et al, 2015;Vendl et al, 2015;Vendl et al, 2016a). In addition, the intra-individual variation in CH 4 emission in domestic ruminants is explained by differences in digesta retention, possibly linked to digestive tract capacity (Pinares-Patiño et al, 2003;Goopy et al, 2014;Cabezas-Garcia et al, 2017).…”

“…Additionally, the combination of an apparent evolution of a high fluid throughput or 'digesta washing' in macropods, and results from various in vitro studies led to an additional hypothesis (Vendl et al, 2015): A large difference in the MRT of fluids and particles (measured as a high MRTparticle: MRTsolute ratio and leading to a high outwash rate of microbes from the fermentation chamber) might create conditions favourable of a microbiome tuned towards growth rather than CH 4 production. However, in spite of a similar pattern of fluid and particle retention in pygmy hippos as in macropods (Supplementary Material Figure S4), no similarity in CH 4 emissions were evident between these species.…”

CH4/CO2 Ratios and Carbon Isotope Enrichment Between Diet and Breath in Herbivorous Mammals

“…Possibly, this is linked to a rhythm of rumen gas eructation that is of a lesser frequency than the animal's regular breathing frequency. Whether similar between-breath variation should be expected for other foregut fermenters in addition to demonstrated diurnal irregularities (Vendl et al, 2015), and to what degree CH 4 produced in the hindgut will be excreted by flatulence vs. absorption in the blood and exhalation, remains to be investigated. Although it is well established that CH 4 produced in the hindgut is also exhaled in breath (McKay et al, 1985;Sasaki et al, 1999), the contribution of flatulence to overall CH 4 remains unexplored in non-ruminants, and even in respiration chambers.…”

Merycism in western grey (Macropus fuliginosus) and red kangaroos (Macropus rufus)

“…In the recovery phases of a feeding experiment with western grey (Macropus fuliginosus) and red 84 kangaroos (Macropus rufus) (Vendl et al, 2015), we noted the repeated occurrence of merycism and 85 decided to record the behaviour as systematically as possible under the conditions of that experiment 86 by video documentation. This contribution therefore does not represent an experimental investigation 87 of merycism in macropods, but a systematic evaluation of a series of anecdotal observations.…”