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Methane emissions of geese (Anser anser) and turkeys (Meleagris gallopavo) fed pelleted lucerne
Comparative Biochemistry and Physiology, Part A 242 (2020) 110651
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Methane emissions of geese (Anser anser) and turkeys (Meleagris gallopavo) fed pelleted lucerne
T
Marcus Claussa, , Samuel Freia, Jean-Michel Hatta, Michael Kreuzerb ⁎
a b
Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Winterthurerstr. 260, 8057 Zurich, Switzerland ETH Zurich, Institute of Agricultural Sciences, Universitätsstr. 2, 8092 Zurich, Switzerland
ARTICLE INFO
ABSTRACT
Keywords: Avian herbivore Poultry Caeca Uric acid Digestion
In contrast to mammalian herbivores, birds are generally perceived to produce little methane (CH4) during digestion, and accounting for poultry in greenhouse gas inventories is considered unnecessary. We measured CH4 emissions in six domestic geese (Anser anser, 5.0 ± 0.9 kg) and six domestic turkeys (Meleagris gallopavo, 6.3 ± 0.6 kg) kept on a diet of lucerne pellets only, using open-circuit chamber respirometry. Measurements of oxygen consumption were similar to previously published values in these species. Absolute CH4 emissions per day were lower in geese (0.58 ± 0.10 L) than in turkeys (1.48 ± 0.16 L) and represented 0.4 ± 0.2 and 0.6 ± 0.1% of gross energy intake, respectively. These results confirm previous findings on the presence of methanogenes in the digestive tract of poultry species, and in vitro measurements performed on poultry caecal contents. In relation to mammalian herbivores in terms of absolute CH4 emissions, CH4 yield per dry matter or gross energy intake, or the CH4:CO2 ratio, the lucerne-fed geese and turkeys had comparatively low values. The emission of CH4 in spite of the very short digesta retention times and low fibre digestibility, as measured in the same animals, gives rise to the hypothesis that that in some birds, caecal fermentation and the associated CH4 production may be related to the microbial digestion of uric acid. The hypothesis that CH4 emissions in poultry may depend not only on dietary fibre but also on dietary digestible protein (that is excreted as uric acid in urine and retrogradely transported from the cloaca into the caeca) remains to be tested.
1. Introduction Herbivorous birds produce methane (CH4). This is known from in vitro experiments in ratites, Anseriformes and Galliformes using faeces (Hackstein and Van Alen, 1996; Saengkerdsub et al., 2007) or caecal content (Shrimpton, 1966; Marounek and Rada, 1998; Fievez et al., 2001; Saengkerdsub et al., 2006; Chen et al., 2014). Methane production was also demonstrated by spot-sampling air from rock ptarmigans (Lagopus mutus), ducks (Cairina moschata) and geese (Anser anser) kept in closed-circuit respiration chambers (Gasaway, 1976; Chen et al., 2003; Chen et al., 2014). By contrast, continuous measurements in open-circuit respiration systems are rare. The few measurements allowing extrapolations for daily CH4 emissions in birds seemed to indicate extremely low levels of CH4 (reviewed in Fritz et al., 2012). The to our knowledge only open-circuit respiration measurements of CH4 in chickens (Gallus gallus) (Hadorn and Wenk, 1996a, 1996b) support this impression. However, recent open-circuit measurements suggest that at least ratites (ostriches Struthio camelus, emus Dromaius novaehollandiae, and rheas Rhea americana) produce CH4 in magnitudes expected of
⁎
similar-sized nonruminant mammalian herbivores (Frei et al., 2015a; Frei et al., 2015b). It is generally assumed that CH4 production is mainly related to microbial fibre digestion, and a substantial fibre degradation is in turn dependent on prolonged digesta retention (Stevens and Hume, 1998). Therefore, it may appear astonishing that avian species such as geese or emus, with poor fibre digestion and very short digesta retention times (Frei et al., 2015c; Frei et al., 2017), are nevertheless among the CH4producing birds (Hackstein and Van Alen, 1996; Frei et al., 2015b). By comparing caecotomized and intact geese, Chen et al. (2003) demonstrated that the caeca are the main origin of CH4 in this and, given the in vitro studies mentioned above, probably also other avian species. Methanogenic archaea have been detected in the digestive tracts of chicken, geese and turkeys (Meleagris gallopavo) (Miller and Wolin, 1986). Nevertheless, the most recent version of the guidelines for national greenhouse gas inventories (IPCC, 2006) still does not take domestic poultry into account, most likely because of the very low levels of dietary fibre in commercial poultry diets, and the literature reports on generally low avian CH4 emissions mentioned above.
Corresponding author. E-mail address: [email protected] (M. Clauss).
https://doi.org/10.1016/j.cbpa.2020.110651 Received 23 October 2019; Received in revised form 26 November 2019; Accepted 6 January 2020 Available online 07 January 2020 1095-6433/ © 2020 Elsevier Inc. All rights reserved.
Comparative Biochemistry and Physiology, Part A 242 (2020) 110651
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In order to increase available in vivo CH4 measurements, and to further explore potential differences between mammals and birds in relation to CH4 emissions, we performed open-circuit respiration measurements in geese and turkeys as part of a study that measured intake, digestion and digesta retention on a diet of pelleted lucerne in these species (Frei et al., 2017). For the two investigated species, we hypothesised that turkeys would produce more CH4 than geese because of their more voluminous caeca and longer digesta retention times (Frei et al., 2017).
Table 1 Average ( ± standard deviation) methane (CH4) respiration measures in geese (Anser anser) and turkeys (Meleagris gallopavo).
2. Materials and methods
Measure
Unit
Goose (n = 6)
Turkey (n = 6)
Body mass (BM) CH4
[kg] [L/day] [L/kg BM/day] [L/kg DMI] [% GEI] [% DEI] [L/kg dNDFi] ratio
5.0 ± 0.9a 0.58 ± 0.10a 0.12 ± 0.02a 1.7 ± 0.8 0.4 ± 0.2 1.2 ± 0.6 40.1 ± 20.6 0.011 ± 0.002a
6.3 ± 0.6b 1.48 ± 0.16b 0.24 ± 0.04b 2.6 ± 0.6 0.6 ± 0.1 1.6 ± 0.2 35.9 ± 9.3 0.017 ± 0.002b
CH4:CO2
GEI gross energy intake, DEI digestible energy intake, DMI dry matter intake; dNDFi intake of digestible neutral detergent fibre. Within lines, different superscripts indicate significant differences (P < .05) by independent samples t-test.
The general animal husbandry and experimental setup of this study was described previously in Frei et al. (2017), in which intake, digestibility and digesta passage measured in the same animals was reported. The study was performed with approval of the Swiss Cantonal Animal Care and Use Committee Zurich and was carried out under the animal experiment licence no. 142/2011. Six domestic geese (hybrid) and six domestic turkeys (Kelly-Bronze), all subadult, were kept on an exclusive ad libitum diet of pelleted alfalfa (Medicago sativa) (nutrient composition given in Frei et al., 2017; crude protein 15% and neutral detergent fibre 45% in dry matter). The diet was fed for 21 days (14 days of adaptation period followed by 7 days of experiment). Drinking water was also available at ad libitum access. The animals were kept individually for the last 3 days of the adaptation period and the entire 7-day collection period. On day 6 of the collection period, the birds were weighed and moved individually for 23 h into respiration chambers (1.0 × 0.6 × 0.7 m). As for other species in the same series of experiments (Frei et al., 2015a, 2015b), the chambers were custom-made on site out of wood, with a fabric carpet flooring, and gaps were covered with construction tape or sealed with silicon. The carpet floors were covered with straw to provide a comfortable and warm bedding. The chambers were equipped with 10 × 20 cm acrylic glass windows to facilitate monitoring of the animals. Water and pelleted lucerne were provided for ad libitum consumption. Chambers were constantly and unidirectionally ventilated by a pull-through system where ambient air entered the chamber through a series of air inlets at the bottom, mixed passively with the chamber air and was then pulled out through a series of air outlets on the roof by a pump (Flowkit 100, Sable Systems, Las Vegas, USA). A constant airflow of 18.4 to 24.2 L/min for geese and 24.1 to 27.8 L/min for turkeys was applied. Both, the flow and the
composition of the outgoing air, and the composition of ambient air (as baseline), were measured in alternating 60 s intervals. The gas concentrations were measured by O2 and CO2 analysers (Turbofox, Sable Systems) as well as by a CH4 analyser (MA-10, Sable Systems), and data were automatically adjusted for barometric pressure, water vapour pressure and air flow rates, which were constantly recorded during respirometry (Turbofox, Sable Systems). The gas analysers were calibrated prior to each measurement by using pure N2 gas and a span gas (PanGas, Dagmarsellen, Switzerland; 19.91% O2, 0.51% CO2 and 0.49% CH4 dissolved in N2). The data were analysed with the software ExpeData (Sable Systems) for O2 consumed and CO2 as well as CH4 emitted after correcting for concentrations in ambient air. The overall metabolic rate (MR) per individual was calculated by multiplying the amount of O2 consumed (in L) by 20.08 kJ/L (based on McNab, 2008), accounting for the entire stay inside the respiration chamber and therefore including all activities inside the chamber (such as standing, resting, feeding). The resting metabolic rate (RMR) was estimated using the average of the 20 lowest O2 measurement data points of each animal within the 23-h period (adapted from Derno et al., 2005). Volume measures of CH4 were transformed into energy by the conversion factor 39.57 kJ/L (Brouwer, 1965). Statistical analyses were performed in SPSS 23.0 (IBM, Armonk, NY, USA). Comparisons between species were made with the parametric ttest or the nonparametric U test, depending on whether normality of data was confirmed or not by the Kolmogorov-Smirnov-test. To account
Goose
A
Turkey
0.08
0.10 0.09
0.07
0.08 0.07 0.06 L/min
L/min
0.06 0.05
0.04
0.04
0.03 0.02
0.03 0.02 10:07
0.05
O2 consumption
14:17
18:27
22:37 Time
2:47
O2 consumption
0.01
CO2 production
0.00 10:07
6:57
CO2 production 14:17
18:27
22:37 Time
2:47
6:57
14:17
18:27
22:37 Time
2:47
6:57
B CH4 (L/min)
CH4 (L/min)
0.003
0.000 10:07
14:17
18:27
22:37 Time
2:47
0.003
0.000 10:07
6:57
Fig. 1. Examples of the results of the respiration measurements for (A) oxygen and carbon dioxide and (B) methane in one goose (Anser anser) and one turkey (Meleagris gallopavo) individual, respectively. 2
Comparative Biochemistry and Physiology, Part A 242 (2020) 110651
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Fig. 2. Methane (CH4) emissions of birds (including the geese and turkey of the present study) (A) absolute amount in relation to body mass; (B) the CH4:carbon dioxide (CO2) ratio in relation to body mass; (C) CH4 yield (per dry matter intake) in relation to the daily relative dry matter intake (per metabolic body weight). Comparative data for ratite birds from Frei et al. (2015a, 2015b), for mammals from Clauss et al. (2020), and for tortoises from Franz et al. (2011).
A 1000 100
CH4 (L/d)
10 for the effect of relative dry matter intake (in g/kg0.75/d) on CH4 yield, we performed a General Linear Model (GLM) with CH4 yield as the dependent variable, the relative food intake as the independent variable, and species as a cofactor. First, a GLM including the relative intake × species interaction was performed, confirming that the interaction was not significant; then, the GLM was repeated without the interaction. Residuals calculated by the GLM analysis were always normally distributed. The significance level was set to P < .05. We compared our results with previously reported data for birds measured on the same diet as used in the present experiment (Frei et al., 2015a; Frei et al., 2015b) and with data from mammals (compiled in Clauss et al., 2020).
1 0.1
Ruminants Nonruminants Tortoises Ostrich Rhea Emu Goose Turkey
0.01 0.001 0.5
5
50 Body mass (kg)
500
B 0.12
3. Results
Ruminants Nonruminants Ostrich Rhea Emu Goose Turkey
0.10
The respiration measurements indicated ultradian fluctuation not only in the consumption of O2 and emission of CO2 (Fig. 1 AB), but also in the emission of CH4 (Fig. 1 CD). The turkeys emitted significantly higher absolute amounts of CH4 than the geese (Table 1). The difference was also significant when relating CH4 emission to body mass (Fig. 2A), or to the amount of CO2 emitted (Fig. 2B). Although turkeys were heavier than geese, food intake did not differ significantly between the two species (Frei et al., 2017). Still the turkeys had numerically higher CH4 yields (per unit dry matter intake, and per ingested gross energy) than the geese (Fig. 2C), but these data were not normally distributed and the U test did not indicate significant differences (Table 1). The latter was likely due to two geese that had comparatively low intakes, and hence reached CH4 yields in the range of the turkeys. In the preliminary GLM the relative intake × species interaction was not significant (F1,8 = 0.071; P = .514) when relating the relative dry matter intake and species to the CH4 yield. This indicates that the slope of CH4 yield in relation to dry matter intake was the same in the two species. In the model without the interaction, both relative dry matter intake (F1,9 = 24.873; P = .001) and species (F1,9 = 34.126; P < .001) were significant, confirming that turkeys had a higher CH4 yield at similar intake levels than geese. In spite of the generally low neutral detergent fibre (NDF) digestibility of geese and turkeys compared to other herbivorous species, and the observation that geese had an even lower digestibility than turkeys (Frei et al., 2017; Fig. 3A), they were similar to each other in terms of CH4 yield per unit digested NDF, and to other birds and nonruminant mammals (Table 1, Fig. 3B). Still it seems (Fig. 3C) that, at a similar relative digestible NDF intake, turkeys produced more CH4 per unit digested NDF than geese. Also for this variable the relative intake × species interaction was not significant (F1,8 = 0.233; P = .642), indicating that the slope of the relative intake to CH4 yield did not differ between the species. When excluding the interaction, relative digestible NDF intake (F1,9 = 12.159; P = .007) was significantly related to the respective CH4 yield, but there was only a trend for the species effect (F1,9 = 3.608; P = .090). Compared to most other species for which comparative data was available, both geese and turkeys have relatively short digesta retention times (Frei et al., 2017; Fig. 4A). Across the bird species, fibre digestibility was higher in species with longer digesta retention times (Fig. 4B), and across birds and mammals, the CH4 yield (per unit dry matter intake) increased with increasing digesta retention (Fig. 4C). However, this pattern was not evident within the geese (where NDF
CH4:CO2 (L/L)
0.08 0.06 0.04 0.02 0.00 0.5
5
50 Body mass (kg)
500
C 100 Ruminants
CH4 (L/kg DMI)
Nonruminants Ostrich Rhea Emu Goose Turkey
10
1 0
50
100
150
200
250
Relative dry matter intake (g/kg0.75/d)
3
Comparative Biochemistry and Physiology, Part A 242 (2020) 110651
M. Clauss, et al.
Fig. 3. Digestive physiology measures in birds (including the geese and turkey of the present study) (A) neutral detergent fibre (NDF) apparent digestibility in relation to body mass; (B) CH4 yield (per digestible NDF intake) in relation to body mass; (C) CH4 yield (per digestible NDF intake) in relation to the daily relative digestible NDF intake (per metabolic body weight). Comparative data for ratite birds from Frei et al. (2015a, 2015b) and for mammals from Clauss et al. (2020).
A 100 90
NDF digestibility (%)
80 70
digestibility and CH4 yield varied at similar retention times) and not within turkeys (where retention times varied at similar NDF digestibility or CH4 yield) (Fig. 4C).
60 50 40 30
Ruminants Nonruminants Ostrich Rhea
20
4. Discussion The results of the present study confirm previous reports that geese and turkeys produce CH4 (Hackstein and Van Alen, 1996; Chen et al., 2003), and add a quantitative aspect to this fact. They indicate that these species can emit CH4 at a daily magnitude that is similar to that of some similar-sized, nonruminant herbivorous mammals. Together with in vitro reports on CH4 in other poultry species (Marounek et al., 1999; Tsukahara and Ushida, 2000; Saengkerdsub et al., 2006; Saengkerdsub et al., 2007; Chen et al., 2014), they also suggest that a contribution of poultry to CH4 emissions should not be completely excluded. The absence of CH4 in previous respiration experiments in chicken (Jørgensen et al., 1996) is probably explained by the young age of the animals, as CH4 production is evident in chicken caecum contents in vitro only from a one month of age onwards (Marounek and Rada, 1998). From this point of view, and from the aspect of age-related growth and use or excretion of digestible protein, more detailed characterisation of the growth stage of the animals used in this study, and a variety of age groups would have been welcome. As already mentioned in previous studies using the same setup, the nature of the on-site respiratory chambers prevented the traditional gas recovery tests by burning (Frei et al., 2015b). Nevertheless, the recorded O2 consumption measurements using this system show a high degree of correspondence to previously published data (Frei et al., 2015a, 2015b; and Table 2) and thus suggest reliability of the data. Notably, a hypothetical restriction in gas recovery would make the O2 measurements over-, and the CH4 measurements underestimates, which would not change the qualitative relevance of our results. It has been reported previously that for turkeys, no adaptation to the respiration chamber confinement is necessary for reliable measurements (MacLeod et al., 1985); this in contrast to chicken where a training effect was observed (Misson, 1974). To our knowledge, no similar observations exist for geese. The lower respiratory quotient of the geese when compared to the turkeys in the present study (Table 2) might suggest that, in contrast to turkeys, geese were more stressed in the respiration chambers and did not consume the available food as reliably and used more body fat reserves to cover energy requirements. Nevertheless, the oxygen measurements and the corresponding derived metabolic rates of the present study were of similar magnitudes as those reported previously for geese and turkey (Table 2), suggesting that our measurements were plausible. Additionally, the well-described pattern of reduced metabolism at night in chicken (Macleod et al., 1980) was also reflected in the poultry species of the present study. Typical patterns related to CH4 physiology known from mammals were also evident in the avian data. There was a negative relationship between the relative intake level and the CH4 yield per unit dry matter intake in domestic ruminants (Pinares-Patiño et al., 2003; Hammond et al., 2014; Cabezas-Garcia et al., 2017) or macropods (Vendl et al., 2015). A similar relationship was described for ratite birds (Frei et al., 2015b), and was evident both within the avian species of the present
Emu Goose Turkey
10 0 0.5
5
50 Body mass (kg)
500
B
CH4 (L/kg dNDFI)
1000
100
10
Ruminants Nonruminants Ostrich Rhea Emu Goose Turkey
1 0.5
5
50
500
Body mass (kg)
C
CH4 (L/kg dNDFI)
1000
100
10 Ruminants Nonruminants Ostrich Rhea Emu Goose Turkey
1 0
5
10
15
20
25
Relative digestible NDF intake (g/kg0.75/d)
4
Comparative Biochemistry and Physiology, Part A 242 (2020) 110651
M. Clauss, et al.
Fig. 4. Digestive physiology measures in birds (including the geese and turkey of the present study) (A) particle mean retention time (MRT) in relation to body mass; (B) neutral detergent fibre (NDF) apparent digestibility in relation to MRT; (C) CH4 yield (per dry matter intake) in relation to MRT. Comparative data for birds from Frei et al. (2015a, 2015b, 2015c, 2017) and for mammals from Clauss et al. (2020).
A
Mean retention time (h)
100
study, and across all avian species (Fig. 2C). Similarly, the negative relationship between the relative intake of digestible fibre and the CH4 yield per unit digested fibre, reported for mammalian herbivores (Clauss et al., 2020), was evident in birds as well (Fig. 3C). Finally, positive relationships between digesta retention times and either fibre digestibility or CH4 yield per unit dry matter intake were also registered in the avian species (Fig. 4 BC). It should be noted that in all these comparative datasets, the avian species measured so far are at the lower end of the range of CH4 measurements. Pending further in vivo measurements, this suggests that in general the digestive physiology of birds does not comprise the high-CH4 yielding microbiome action observed in various herbivorous mammalian species (Clauss et al., 2020). Nevertheless, relevant differences in general microbial fermentation and hence also CH4 physiology seem to exist between bird species, and also between poultry species and mammals. As reviewed in Frei et al. (2017), there is a retrograde transport of urine, including uric acid, in a number of avian species, including geese and turkeys. Uric acid may actually represent a major fermentation substrate for the caecal microbiome (Braun and Campbell, 1989; Mead, 1989). The extent to which CH4 production is linked to uric acid fermentation has, to our knowledge, not been investigated so far. Differences in the caecum size between turkeys and geese could also be related to the extent of retrograde urine transport into the caeca, and could be behind the increased CH4 emission in turkeys. Uric acid production does not depend on fibre but on digestible protein intake (Hevia and Clifford, 1977). This may mean that CH4 production may be significant even in birds fed diets rich in digestible protein and thus leading to high levels of uric acid in the urine and, after retrograde transport, in the caeca. This hypothesis matches the observations of Tsukahara and Ushida (2000) that CH4 production in chicken caecal content was higher on a meat- than a plant-based diet. It also matches the observations of Chen et al. (2014) that the addition of lucerne meal (with putatively less digestible protein) to a standard grower diet reduced CH4 production in the caecum contents of geese and ducks, even though the reasons for this reduction remain unknown. Finally, it also matches the observation that in chicken, the addition of fibre-rich components to a basal diet did not increase CH4 emissions (Hadorn and Wenk, 1996a, 1996b). Uric acid is a nitrogenous substance with a carbohydrate moiety; such substrates have been shown to be susceptible to microbial degradation that includes the production of CH4 (Marounek et al., 2000). Actually, the presence of non‑nitrogenous fermentable carbohydrates, such as fibre, when replacing digestible protein, might therefore reduce CH4 emissions in some avian species. To conclude, birds should not be overlooked as a potential source for CH4 emissions. However, before estimation instructions for poultry are included in the guidelines for national greenhouse gas inventories (IPCC, 2006), additional studies are required to corroborate our findings. In particular, the different ages until which poultry are typically used must be considered, as a large proportion of poultry is slaughtered at a very young age that might preclude relevant CH4 emissions. Additionally, it must be confirmed by direct comparison to which extent poultry, similar to mammalian herbivores and omnivores, produce less CH4 when maintained on low-fibre concentrates, like the typical poultry feeds. Alternatively, the different fermentation substrate in the avian caeca, uric acid deriving from protein metabolism, might result in poultry CH4 emissions reacting less to dietary fibre than to dietary digestible protein levels.
10
Ruminants Nonruminants Ostrich Rhea Emu Goose Turkey
1 0.5
5
50 Body mass (kg)
500
B 100
aD NDF (%)
80
60
40 Ruminants Nonruminants Ostrich Rhea Emu Goose Turkey
20
0 0
10
20
30
40
50
60
70
Mean retention time (h)
C
CH4 (L/kg DMI)
100
10 Ruminants Nonruminants Ostrich Rhea Emu Goose Turkey
1 0
10
20
30
40
50
60
70
Mean retention time (h)
5
Comparative Biochemistry and Physiology, Part A 242 (2020) 110651
M. Clauss, et al.
Table 2 Metabolic rate measurements based on oxygen consumption (mean ± SD) in geese (Anser anser) and turkeys (Meleagris gallopavo). Species
n
Diet
Body mass
RQ
6
Lucerne Fasted
Turkey
6
Lucerne Fasted T / fasted Fasted Fasted Fasted
5 15 4/4 9
5.0 ± 0.9 3.2 5.0 5.8 6.3 ± 0.6 3.9 13.1 5.6 / 4.6 9.7 / 4.4 4.7
RMR
BMR
Method of respirometry
Reference
Chamber Chamber Chamber
Present study Giaja (1931) Benedict and Lee (1937), cited in King and Farner (1961) Herzog (1930) Present study Giaja (1931) MacLeod et al. (1985)a Gray and Prince (1988)b Oberlag et al. (1990)c Haroldson et al. (1998)d
———————————— [kJ/kg0.75/day] ——————————
[kg] Geese
MR
0.80 ± 0.15
424 ± 115
334 ± 84
0.99 ± 0.05
460 ± 39
356 ± 37
0.98 / 0.72
366 / 354
313–338
373 350 319 325 313–338 249 / 299 350 / 323 262
Chamber Chamber Chamber Chamber Chamber Chamber Chamber
T commercial turkey diet, Mix mixed diet of pellets, fruits, lettuce and bread, RQ respiratory quotient calculated as CO2/O2, MR metabolic rate, SMR standing metabolic rate, RMR resting metabolic rate, BMR basal metabolic rate. a Metabolic rates re-calculated from data on heat production and RQ, and RMR/BMR read from graph; RMR/BMR was not different between fed/fasted birds in that study. b Wild turkey males and females, averages for summer and winter. c Wild turkey males and females, averages from measurements in four different seasons. d Wild turkey females.
Acknowledgements
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We thank Geflügel Gourmet AG for access to geese and turkeys. This study was part of project 310030_135252/1 funded by the Swiss National Science Foundation and by the Basle Foundation for Biological Research. Declaration of Competing Interest None. References Braun, E.J., Campbell, C.E., 1989. Uric acid decomposition in the lower gastrointestinal tract. J. Exp. Zool. 252 (Suppl. 3), 70–74. Brouwer, E., 1965. Report of sub-committee on constants and factors. In: Blaxter, K. (Ed.), Energy Metabolism. Academic Press, London, UK, pp. 441–443. Cabezas-Garcia, E.H., Krizsan, S.J., Shingfield, K.J., Huhtanen, P., 2017. Between-cow variation in digestion and rumen fermentation variables associated with methane production. J. Dairy Sci. 100, 4409–4424. Chen, Y.H., Wang, S.Y., Hsu, J.C., 2003. Effect of caecotomy on body weight gain, intestinal characteristics and enteric gas production in goslings. Asian-Austr. J. Anim. Sci. 16, 1030–1034. Chen, Y.H., Lee, S.M., Hsu, J.C., Chang, Y.C., Wang, S.Y., 2014. Methane generation from the intestine of Muscovy ducks, mule ducks and white Roman geese. Aerosol Air Qual. Res. 14, 323–329. Clauss, M., Dittmann, M.T., Vendl, C., Hagen, K.B., Frei, S., Ortmann, S., Müller, D.W.H., Hammer, S., Munn, A.J., Schwarm, A., Kreuzer, M., 2020. Comparative methane production in mammalian herbivores. Animal. https://doi.org/10.1017/ S1751731119003161. (in press). Derno, M., Jentsch, W., Schweigel, M., Kuhla, S., Metges, C.C., Matthes, H.D., 2005. Measurements of heat production for estimation of maintenance energy requirements of Hereford steers. J. Anim. Sci. 83, 2590–2597. Fievez, V., Mbanzamihigo, L., Piattoni, F., Demeyer, D., 2001. Evidence for reductive acetogenesis and its nutritional significance in ostrich hindgut as estimated from in vitro incubations. J. Anim. Physiol. Anim. Nutr. 85, 271–280. Franz, R., Soliva, C.R., Kreuzer, M., Hatt, J.-M., Furrer, S., Hummel, J., Clauss, M., 2011. Methane output of tortoises: its contribution to energy loss related to herbivore body mass. PLoS One 6, e17628. Frei, S., Dittmann, M.T., Reutlinger, C., Ortmann, S., Hatt, J.-M., Kreuzer, M., Clauss, M., 2015a. Methane emission by adult ostriches (Struthio camelus). Comp. Biochem. Physiol. A 180, 1–5. Frei, S., Hatt, J.-M., Ortmann, S., Kreuzer, M., Clauss, M., 2015b. Comparative methane emission by ratites: differences in food intake and digesta retention level out methane production. Comp. Biochem. Physiol. A 188, 70–75. Frei, S., Ortmann, S., Reutlinger, C., Kreuzer, M., Hatt, J.-M., Clauss, M., 2015c. Comparative digesta retention patterns in ratites. Auk Ornithol. Adv. 132, 119–131. Frei, S., Ortmann, S., Kreuzer, M., Hatt, J.-M., Clauss, M., 2017. Digesta retention patterns in geese (Anser anser) and turkeys (Meleagris gallopavo) and deduced function of avian caeca. Comp. Biochem. Physiol. A 204, 219–227.
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M. Clauss, et al. Misson, B.H., 1974. An open circuit respirometer for metabolic studies on the domestic fowl: establishment of standard operating conditions. Br. Poult. Sci. 15, 287–297. Oberlag, D.F., Pekins, P.J., Mautz, W.W., 1990. Influence of seasonal temperatures on wild turkey metabolism. J. Wildl. Manag. 54, 663–667. Pinares-Patiño, C.S., Ulyatt, M.J., Lassey, K.R., Barry, T.N., Holmes, C.W., 2003. Rumen function and digestion parameters associated with differences between sheep in methane emissions when fed chaffed lucerne hay. J. Agric. Sci. 140, 205–214. Saengkerdsub, S., Kim, W.K., Anderson, R.C., Nisbet, D.J., Ricke, S.C., 2006. Effects of nitrocompounds and feedstuffs on in vitro methane production in chicken cecal contents and rumen fluid. Anaerobe 12, 85–92. Saengkerdsub, S., Herrera, P., Woodward, C.L., Anderson, R.C., Nisbet, D.J., Ricke, S.C., 2007. Detection of methane and quantification of methanogenic archaea in faeces from young broiler chickens using real-time PCR. Lett. Appl. Microbiol. 45, 629–634.
Shrimpton, D.H., 1966. Metabolism of the intestinal microflora in birds and its possible influence on the composition of flavour precursors in their muscles. J. Appl. Bacteriol. 29, 222–230. Stevens, C.E., Hume, I.D., 1998. Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol. Rev. 78, 393–427. Tsukahara, T., Ushida, K., 2000. Effects of animal or plant protein diets on cecal fermentaion in Guinea pigs (Cavia porcellus), rats (Rattus norvegicus) and chicks (Gallus gallus domesticus). Comp. Biochem. Physiol. A 127, 139–146. Vendl, C., Clauss, M., Stewart, M., Leggett, K., Hummel, J., Kreuzer, M., Munn, A., 2015. Decreasing methane yield with increasing food intake keeps daily methane emissions constant in two foregut fermenting marsupials, the western grey kangaroo and red kangaroo. J. Exp. Biol. 218, 3425–3434.
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Comparative Biochemistry and Physiology, Part A journal homepage: www.elsevier.com/locate/cbpa
Methane emissions of geese (Anser anser) and turkeys (Meleagris gallopavo) fed pelleted lucerne
T
Marcus Claussa, , Samuel Freia, Jean-Michel Hatta, Michael Kreuzerb ⁎
a b
Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Winterthurerstr. 260, 8057 Zurich, Switzerland ETH Zurich, Institute of Agricultural Sciences, Universitätsstr. 2, 8092 Zurich, Switzerland
ARTICLE INFO
ABSTRACT
Keywords: Avian herbivore Poultry Caeca Uric acid Digestion
In contrast to mammalian herbivores, birds are generally perceived to produce little methane (CH4) during digestion, and accounting for poultry in greenhouse gas inventories is considered unnecessary. We measured CH4 emissions in six domestic geese (Anser anser, 5.0 ± 0.9 kg) and six domestic turkeys (Meleagris gallopavo, 6.3 ± 0.6 kg) kept on a diet of lucerne pellets only, using open-circuit chamber respirometry. Measurements of oxygen consumption were similar to previously published values in these species. Absolute CH4 emissions per day were lower in geese (0.58 ± 0.10 L) than in turkeys (1.48 ± 0.16 L) and represented 0.4 ± 0.2 and 0.6 ± 0.1% of gross energy intake, respectively. These results confirm previous findings on the presence of methanogenes in the digestive tract of poultry species, and in vitro measurements performed on poultry caecal contents. In relation to mammalian herbivores in terms of absolute CH4 emissions, CH4 yield per dry matter or gross energy intake, or the CH4:CO2 ratio, the lucerne-fed geese and turkeys had comparatively low values. The emission of CH4 in spite of the very short digesta retention times and low fibre digestibility, as measured in the same animals, gives rise to the hypothesis that that in some birds, caecal fermentation and the associated CH4 production may be related to the microbial digestion of uric acid. The hypothesis that CH4 emissions in poultry may depend not only on dietary fibre but also on dietary digestible protein (that is excreted as uric acid in urine and retrogradely transported from the cloaca into the caeca) remains to be tested.
1. Introduction Herbivorous birds produce methane (CH4). This is known from in vitro experiments in ratites, Anseriformes and Galliformes using faeces (Hackstein and Van Alen, 1996; Saengkerdsub et al., 2007) or caecal content (Shrimpton, 1966; Marounek and Rada, 1998; Fievez et al., 2001; Saengkerdsub et al., 2006; Chen et al., 2014). Methane production was also demonstrated by spot-sampling air from rock ptarmigans (Lagopus mutus), ducks (Cairina moschata) and geese (Anser anser) kept in closed-circuit respiration chambers (Gasaway, 1976; Chen et al., 2003; Chen et al., 2014). By contrast, continuous measurements in open-circuit respiration systems are rare. The few measurements allowing extrapolations for daily CH4 emissions in birds seemed to indicate extremely low levels of CH4 (reviewed in Fritz et al., 2012). The to our knowledge only open-circuit respiration measurements of CH4 in chickens (Gallus gallus) (Hadorn and Wenk, 1996a, 1996b) support this impression. However, recent open-circuit measurements suggest that at least ratites (ostriches Struthio camelus, emus Dromaius novaehollandiae, and rheas Rhea americana) produce CH4 in magnitudes expected of
⁎
similar-sized nonruminant mammalian herbivores (Frei et al., 2015a; Frei et al., 2015b). It is generally assumed that CH4 production is mainly related to microbial fibre digestion, and a substantial fibre degradation is in turn dependent on prolonged digesta retention (Stevens and Hume, 1998). Therefore, it may appear astonishing that avian species such as geese or emus, with poor fibre digestion and very short digesta retention times (Frei et al., 2015c; Frei et al., 2017), are nevertheless among the CH4producing birds (Hackstein and Van Alen, 1996; Frei et al., 2015b). By comparing caecotomized and intact geese, Chen et al. (2003) demonstrated that the caeca are the main origin of CH4 in this and, given the in vitro studies mentioned above, probably also other avian species. Methanogenic archaea have been detected in the digestive tracts of chicken, geese and turkeys (Meleagris gallopavo) (Miller and Wolin, 1986). Nevertheless, the most recent version of the guidelines for national greenhouse gas inventories (IPCC, 2006) still does not take domestic poultry into account, most likely because of the very low levels of dietary fibre in commercial poultry diets, and the literature reports on generally low avian CH4 emissions mentioned above.
Corresponding author. E-mail address: [email protected] (M. Clauss).
https://doi.org/10.1016/j.cbpa.2020.110651 Received 23 October 2019; Received in revised form 26 November 2019; Accepted 6 January 2020 Available online 07 January 2020 1095-6433/ © 2020 Elsevier Inc. All rights reserved.
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In order to increase available in vivo CH4 measurements, and to further explore potential differences between mammals and birds in relation to CH4 emissions, we performed open-circuit respiration measurements in geese and turkeys as part of a study that measured intake, digestion and digesta retention on a diet of pelleted lucerne in these species (Frei et al., 2017). For the two investigated species, we hypothesised that turkeys would produce more CH4 than geese because of their more voluminous caeca and longer digesta retention times (Frei et al., 2017).
Table 1 Average ( ± standard deviation) methane (CH4) respiration measures in geese (Anser anser) and turkeys (Meleagris gallopavo).
2. Materials and methods
Measure
Unit
Goose (n = 6)
Turkey (n = 6)
Body mass (BM) CH4
[kg] [L/day] [L/kg BM/day] [L/kg DMI] [% GEI] [% DEI] [L/kg dNDFi] ratio
5.0 ± 0.9a 0.58 ± 0.10a 0.12 ± 0.02a 1.7 ± 0.8 0.4 ± 0.2 1.2 ± 0.6 40.1 ± 20.6 0.011 ± 0.002a
6.3 ± 0.6b 1.48 ± 0.16b 0.24 ± 0.04b 2.6 ± 0.6 0.6 ± 0.1 1.6 ± 0.2 35.9 ± 9.3 0.017 ± 0.002b
CH4:CO2
GEI gross energy intake, DEI digestible energy intake, DMI dry matter intake; dNDFi intake of digestible neutral detergent fibre. Within lines, different superscripts indicate significant differences (P < .05) by independent samples t-test.
The general animal husbandry and experimental setup of this study was described previously in Frei et al. (2017), in which intake, digestibility and digesta passage measured in the same animals was reported. The study was performed with approval of the Swiss Cantonal Animal Care and Use Committee Zurich and was carried out under the animal experiment licence no. 142/2011. Six domestic geese (hybrid) and six domestic turkeys (Kelly-Bronze), all subadult, were kept on an exclusive ad libitum diet of pelleted alfalfa (Medicago sativa) (nutrient composition given in Frei et al., 2017; crude protein 15% and neutral detergent fibre 45% in dry matter). The diet was fed for 21 days (14 days of adaptation period followed by 7 days of experiment). Drinking water was also available at ad libitum access. The animals were kept individually for the last 3 days of the adaptation period and the entire 7-day collection period. On day 6 of the collection period, the birds were weighed and moved individually for 23 h into respiration chambers (1.0 × 0.6 × 0.7 m). As for other species in the same series of experiments (Frei et al., 2015a, 2015b), the chambers were custom-made on site out of wood, with a fabric carpet flooring, and gaps were covered with construction tape or sealed with silicon. The carpet floors were covered with straw to provide a comfortable and warm bedding. The chambers were equipped with 10 × 20 cm acrylic glass windows to facilitate monitoring of the animals. Water and pelleted lucerne were provided for ad libitum consumption. Chambers were constantly and unidirectionally ventilated by a pull-through system where ambient air entered the chamber through a series of air inlets at the bottom, mixed passively with the chamber air and was then pulled out through a series of air outlets on the roof by a pump (Flowkit 100, Sable Systems, Las Vegas, USA). A constant airflow of 18.4 to 24.2 L/min for geese and 24.1 to 27.8 L/min for turkeys was applied. Both, the flow and the
composition of the outgoing air, and the composition of ambient air (as baseline), were measured in alternating 60 s intervals. The gas concentrations were measured by O2 and CO2 analysers (Turbofox, Sable Systems) as well as by a CH4 analyser (MA-10, Sable Systems), and data were automatically adjusted for barometric pressure, water vapour pressure and air flow rates, which were constantly recorded during respirometry (Turbofox, Sable Systems). The gas analysers were calibrated prior to each measurement by using pure N2 gas and a span gas (PanGas, Dagmarsellen, Switzerland; 19.91% O2, 0.51% CO2 and 0.49% CH4 dissolved in N2). The data were analysed with the software ExpeData (Sable Systems) for O2 consumed and CO2 as well as CH4 emitted after correcting for concentrations in ambient air. The overall metabolic rate (MR) per individual was calculated by multiplying the amount of O2 consumed (in L) by 20.08 kJ/L (based on McNab, 2008), accounting for the entire stay inside the respiration chamber and therefore including all activities inside the chamber (such as standing, resting, feeding). The resting metabolic rate (RMR) was estimated using the average of the 20 lowest O2 measurement data points of each animal within the 23-h period (adapted from Derno et al., 2005). Volume measures of CH4 were transformed into energy by the conversion factor 39.57 kJ/L (Brouwer, 1965). Statistical analyses were performed in SPSS 23.0 (IBM, Armonk, NY, USA). Comparisons between species were made with the parametric ttest or the nonparametric U test, depending on whether normality of data was confirmed or not by the Kolmogorov-Smirnov-test. To account
Goose
A
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0.08
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B CH4 (L/min)
CH4 (L/min)
0.003
0.000 10:07
14:17
18:27
22:37 Time
2:47
0.003
0.000 10:07
6:57
Fig. 1. Examples of the results of the respiration measurements for (A) oxygen and carbon dioxide and (B) methane in one goose (Anser anser) and one turkey (Meleagris gallopavo) individual, respectively. 2
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Fig. 2. Methane (CH4) emissions of birds (including the geese and turkey of the present study) (A) absolute amount in relation to body mass; (B) the CH4:carbon dioxide (CO2) ratio in relation to body mass; (C) CH4 yield (per dry matter intake) in relation to the daily relative dry matter intake (per metabolic body weight). Comparative data for ratite birds from Frei et al. (2015a, 2015b), for mammals from Clauss et al. (2020), and for tortoises from Franz et al. (2011).
A 1000 100
CH4 (L/d)
10 for the effect of relative dry matter intake (in g/kg0.75/d) on CH4 yield, we performed a General Linear Model (GLM) with CH4 yield as the dependent variable, the relative food intake as the independent variable, and species as a cofactor. First, a GLM including the relative intake × species interaction was performed, confirming that the interaction was not significant; then, the GLM was repeated without the interaction. Residuals calculated by the GLM analysis were always normally distributed. The significance level was set to P < .05. We compared our results with previously reported data for birds measured on the same diet as used in the present experiment (Frei et al., 2015a; Frei et al., 2015b) and with data from mammals (compiled in Clauss et al., 2020).
1 0.1
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3. Results
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0.10
The respiration measurements indicated ultradian fluctuation not only in the consumption of O2 and emission of CO2 (Fig. 1 AB), but also in the emission of CH4 (Fig. 1 CD). The turkeys emitted significantly higher absolute amounts of CH4 than the geese (Table 1). The difference was also significant when relating CH4 emission to body mass (Fig. 2A), or to the amount of CO2 emitted (Fig. 2B). Although turkeys were heavier than geese, food intake did not differ significantly between the two species (Frei et al., 2017). Still the turkeys had numerically higher CH4 yields (per unit dry matter intake, and per ingested gross energy) than the geese (Fig. 2C), but these data were not normally distributed and the U test did not indicate significant differences (Table 1). The latter was likely due to two geese that had comparatively low intakes, and hence reached CH4 yields in the range of the turkeys. In the preliminary GLM the relative intake × species interaction was not significant (F1,8 = 0.071; P = .514) when relating the relative dry matter intake and species to the CH4 yield. This indicates that the slope of CH4 yield in relation to dry matter intake was the same in the two species. In the model without the interaction, both relative dry matter intake (F1,9 = 24.873; P = .001) and species (F1,9 = 34.126; P < .001) were significant, confirming that turkeys had a higher CH4 yield at similar intake levels than geese. In spite of the generally low neutral detergent fibre (NDF) digestibility of geese and turkeys compared to other herbivorous species, and the observation that geese had an even lower digestibility than turkeys (Frei et al., 2017; Fig. 3A), they were similar to each other in terms of CH4 yield per unit digested NDF, and to other birds and nonruminant mammals (Table 1, Fig. 3B). Still it seems (Fig. 3C) that, at a similar relative digestible NDF intake, turkeys produced more CH4 per unit digested NDF than geese. Also for this variable the relative intake × species interaction was not significant (F1,8 = 0.233; P = .642), indicating that the slope of the relative intake to CH4 yield did not differ between the species. When excluding the interaction, relative digestible NDF intake (F1,9 = 12.159; P = .007) was significantly related to the respective CH4 yield, but there was only a trend for the species effect (F1,9 = 3.608; P = .090). Compared to most other species for which comparative data was available, both geese and turkeys have relatively short digesta retention times (Frei et al., 2017; Fig. 4A). Across the bird species, fibre digestibility was higher in species with longer digesta retention times (Fig. 4B), and across birds and mammals, the CH4 yield (per unit dry matter intake) increased with increasing digesta retention (Fig. 4C). However, this pattern was not evident within the geese (where NDF
CH4:CO2 (L/L)
0.08 0.06 0.04 0.02 0.00 0.5
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C 100 Ruminants
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50
100
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Relative dry matter intake (g/kg0.75/d)
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Fig. 3. Digestive physiology measures in birds (including the geese and turkey of the present study) (A) neutral detergent fibre (NDF) apparent digestibility in relation to body mass; (B) CH4 yield (per digestible NDF intake) in relation to body mass; (C) CH4 yield (per digestible NDF intake) in relation to the daily relative digestible NDF intake (per metabolic body weight). Comparative data for ratite birds from Frei et al. (2015a, 2015b) and for mammals from Clauss et al. (2020).
A 100 90
NDF digestibility (%)
80 70
digestibility and CH4 yield varied at similar retention times) and not within turkeys (where retention times varied at similar NDF digestibility or CH4 yield) (Fig. 4C).
60 50 40 30
Ruminants Nonruminants Ostrich Rhea
20
4. Discussion The results of the present study confirm previous reports that geese and turkeys produce CH4 (Hackstein and Van Alen, 1996; Chen et al., 2003), and add a quantitative aspect to this fact. They indicate that these species can emit CH4 at a daily magnitude that is similar to that of some similar-sized, nonruminant herbivorous mammals. Together with in vitro reports on CH4 in other poultry species (Marounek et al., 1999; Tsukahara and Ushida, 2000; Saengkerdsub et al., 2006; Saengkerdsub et al., 2007; Chen et al., 2014), they also suggest that a contribution of poultry to CH4 emissions should not be completely excluded. The absence of CH4 in previous respiration experiments in chicken (Jørgensen et al., 1996) is probably explained by the young age of the animals, as CH4 production is evident in chicken caecum contents in vitro only from a one month of age onwards (Marounek and Rada, 1998). From this point of view, and from the aspect of age-related growth and use or excretion of digestible protein, more detailed characterisation of the growth stage of the animals used in this study, and a variety of age groups would have been welcome. As already mentioned in previous studies using the same setup, the nature of the on-site respiratory chambers prevented the traditional gas recovery tests by burning (Frei et al., 2015b). Nevertheless, the recorded O2 consumption measurements using this system show a high degree of correspondence to previously published data (Frei et al., 2015a, 2015b; and Table 2) and thus suggest reliability of the data. Notably, a hypothetical restriction in gas recovery would make the O2 measurements over-, and the CH4 measurements underestimates, which would not change the qualitative relevance of our results. It has been reported previously that for turkeys, no adaptation to the respiration chamber confinement is necessary for reliable measurements (MacLeod et al., 1985); this in contrast to chicken where a training effect was observed (Misson, 1974). To our knowledge, no similar observations exist for geese. The lower respiratory quotient of the geese when compared to the turkeys in the present study (Table 2) might suggest that, in contrast to turkeys, geese were more stressed in the respiration chambers and did not consume the available food as reliably and used more body fat reserves to cover energy requirements. Nevertheless, the oxygen measurements and the corresponding derived metabolic rates of the present study were of similar magnitudes as those reported previously for geese and turkey (Table 2), suggesting that our measurements were plausible. Additionally, the well-described pattern of reduced metabolism at night in chicken (Macleod et al., 1980) was also reflected in the poultry species of the present study. Typical patterns related to CH4 physiology known from mammals were also evident in the avian data. There was a negative relationship between the relative intake level and the CH4 yield per unit dry matter intake in domestic ruminants (Pinares-Patiño et al., 2003; Hammond et al., 2014; Cabezas-Garcia et al., 2017) or macropods (Vendl et al., 2015). A similar relationship was described for ratite birds (Frei et al., 2015b), and was evident both within the avian species of the present
Emu Goose Turkey
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Fig. 4. Digestive physiology measures in birds (including the geese and turkey of the present study) (A) particle mean retention time (MRT) in relation to body mass; (B) neutral detergent fibre (NDF) apparent digestibility in relation to MRT; (C) CH4 yield (per dry matter intake) in relation to MRT. Comparative data for birds from Frei et al. (2015a, 2015b, 2015c, 2017) and for mammals from Clauss et al. (2020).
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Mean retention time (h)
100
study, and across all avian species (Fig. 2C). Similarly, the negative relationship between the relative intake of digestible fibre and the CH4 yield per unit digested fibre, reported for mammalian herbivores (Clauss et al., 2020), was evident in birds as well (Fig. 3C). Finally, positive relationships between digesta retention times and either fibre digestibility or CH4 yield per unit dry matter intake were also registered in the avian species (Fig. 4 BC). It should be noted that in all these comparative datasets, the avian species measured so far are at the lower end of the range of CH4 measurements. Pending further in vivo measurements, this suggests that in general the digestive physiology of birds does not comprise the high-CH4 yielding microbiome action observed in various herbivorous mammalian species (Clauss et al., 2020). Nevertheless, relevant differences in general microbial fermentation and hence also CH4 physiology seem to exist between bird species, and also between poultry species and mammals. As reviewed in Frei et al. (2017), there is a retrograde transport of urine, including uric acid, in a number of avian species, including geese and turkeys. Uric acid may actually represent a major fermentation substrate for the caecal microbiome (Braun and Campbell, 1989; Mead, 1989). The extent to which CH4 production is linked to uric acid fermentation has, to our knowledge, not been investigated so far. Differences in the caecum size between turkeys and geese could also be related to the extent of retrograde urine transport into the caeca, and could be behind the increased CH4 emission in turkeys. Uric acid production does not depend on fibre but on digestible protein intake (Hevia and Clifford, 1977). This may mean that CH4 production may be significant even in birds fed diets rich in digestible protein and thus leading to high levels of uric acid in the urine and, after retrograde transport, in the caeca. This hypothesis matches the observations of Tsukahara and Ushida (2000) that CH4 production in chicken caecal content was higher on a meat- than a plant-based diet. It also matches the observations of Chen et al. (2014) that the addition of lucerne meal (with putatively less digestible protein) to a standard grower diet reduced CH4 production in the caecum contents of geese and ducks, even though the reasons for this reduction remain unknown. Finally, it also matches the observation that in chicken, the addition of fibre-rich components to a basal diet did not increase CH4 emissions (Hadorn and Wenk, 1996a, 1996b). Uric acid is a nitrogenous substance with a carbohydrate moiety; such substrates have been shown to be susceptible to microbial degradation that includes the production of CH4 (Marounek et al., 2000). Actually, the presence of non‑nitrogenous fermentable carbohydrates, such as fibre, when replacing digestible protein, might therefore reduce CH4 emissions in some avian species. To conclude, birds should not be overlooked as a potential source for CH4 emissions. However, before estimation instructions for poultry are included in the guidelines for national greenhouse gas inventories (IPCC, 2006), additional studies are required to corroborate our findings. In particular, the different ages until which poultry are typically used must be considered, as a large proportion of poultry is slaughtered at a very young age that might preclude relevant CH4 emissions. Additionally, it must be confirmed by direct comparison to which extent poultry, similar to mammalian herbivores and omnivores, produce less CH4 when maintained on low-fibre concentrates, like the typical poultry feeds. Alternatively, the different fermentation substrate in the avian caeca, uric acid deriving from protein metabolism, might result in poultry CH4 emissions reacting less to dietary fibre than to dietary digestible protein levels.
10
Ruminants Nonruminants Ostrich Rhea Emu Goose Turkey
1 0.5
5
50 Body mass (kg)
500
B 100
aD NDF (%)
80
60
40 Ruminants Nonruminants Ostrich Rhea Emu Goose Turkey
20
0 0
10
20
30
40
50
60
70
Mean retention time (h)
C
CH4 (L/kg DMI)
100
10 Ruminants Nonruminants Ostrich Rhea Emu Goose Turkey
1 0
10
20
30
40
50
60
70
Mean retention time (h)
5
Comparative Biochemistry and Physiology, Part A 242 (2020) 110651
M. Clauss, et al.
Table 2 Metabolic rate measurements based on oxygen consumption (mean ± SD) in geese (Anser anser) and turkeys (Meleagris gallopavo). Species
n
Diet
Body mass
RQ
6
Lucerne Fasted
Turkey
6
Lucerne Fasted T / fasted Fasted Fasted Fasted
5 15 4/4 9
5.0 ± 0.9 3.2 5.0 5.8 6.3 ± 0.6 3.9 13.1 5.6 / 4.6 9.7 / 4.4 4.7
RMR
BMR
Method of respirometry
Reference
Chamber Chamber Chamber
Present study Giaja (1931) Benedict and Lee (1937), cited in King and Farner (1961) Herzog (1930) Present study Giaja (1931) MacLeod et al. (1985)a Gray and Prince (1988)b Oberlag et al. (1990)c Haroldson et al. (1998)d
———————————— [kJ/kg0.75/day] ——————————
[kg] Geese
MR
0.80 ± 0.15
424 ± 115
334 ± 84
0.99 ± 0.05
460 ± 39
356 ± 37
0.98 / 0.72
366 / 354
313–338
373 350 319 325 313–338 249 / 299 350 / 323 262
Chamber Chamber Chamber Chamber Chamber Chamber Chamber
T commercial turkey diet, Mix mixed diet of pellets, fruits, lettuce and bread, RQ respiratory quotient calculated as CO2/O2, MR metabolic rate, SMR standing metabolic rate, RMR resting metabolic rate, BMR basal metabolic rate. a Metabolic rates re-calculated from data on heat production and RQ, and RMR/BMR read from graph; RMR/BMR was not different between fed/fasted birds in that study. b Wild turkey males and females, averages for summer and winter. c Wild turkey males and females, averages from measurements in four different seasons. d Wild turkey females.
Acknowledgements
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