Understanding the interaction between the chemistry of forage plants, rumen microbiota, and fermentation, and performance in camel calves can help design suitable feeding strategies that use halophyte plants as alternatives to conventional feeds. The proximate analysis of Atriplex and alfalfa hay in this study followed the range of previous studies [2, 15]. Tannin content of Atriplex was lower than the value indicated in Dadvar et al. [5] and higher than that in Mahipala et al. [16]. In addition to phenols, tannins, and flavonoids, Atriplex contains different antinutritional factors, such as saponins, oxalates, alkaloids, and resins [7]. The tannin and phenols content of alfalfa hay was much lower than Atriplex, and the values indicated by Seyedin et al. [17]. Secondary metabolites in the halophyte plants can modify the rumen microbiota and fermentation [6].
Rumen microbiota and rumen fermentation
The majority of the bacterial community belonged to phyla Bacteroidota and Firmicutes, which agrees with the previous study on tanniniferous plant incubated in camel rumen [6, 7] and Lotus corniculatus [18]. The members of Bacteroidota are specialized in the degradation of polysaccharides such as hemicellulose, cellulose, and pectin [7, 18]. Inclusion of the Atriplex in the camel diet did not affect the relative abundance of phylum Bacteroidota or its dominant family, Prevotellaceae, which indicates that this phylum resists the secondary metabolites of saltbushes (Atriplex) and has a role in the performance of animals [7]. This speculation is supported by the higher prevalence of genus Alloprevotella in Atriplex-fed camels (MM and AA) compared to camels fed alfalfa hay (HH). A similar finding was obtained in lambs fed mimosa condensed tannin [19]. Alloprevotella produces acetate and succinic acid and can enhance rumen fermentation and animal health [20]. Candidate genera Prevotellaceae UCG-003 and Bacteroidales UCG-001 can resist tannins and have potential roles in fiber degradation [21, 22], which demonstrates their higher proportions in Atriplex-fed groups. In contrast, the family Bacteroidales RF16 group declined in group AA fed 100% Atriplex. This family has a potential role in fiber degradation [23].
Some members of the phylum Firmicutes, such as family Ruminococcaceae and genera Acetitomaculum, Moryella, Ruminiclostridium, Christensenellaceae R-7 group, and Anaerovorax, were higher in Atriplex-fed groups. These finding indicates that these bacteria can resist tannins [6, 7]. In addition, these bacteria can degrade fiber and produce VFA such as acetic and butyric acids using H2, which reduces the methane production and improves feed efficiency [13, 24,25,26,27]. Tannin-resistant bacteria contribute to the feed efficiency and ability of camels to utilize thorny bushes, halophytes [6, 7]. In contrast, some fibrolytic bacteria were declined by inclusion of the Atriplex, such as Anaeroplasma [28].
Moreover, some minor phyla were increased in Atriplex-fed calves, including Elusimicrobiota, Actinobacteriota, and Planctomycetota. The members of these phyla can resist tannins [6, 7, 13, 29] and ferment glucose and complex carbohydrates to acetic and lactic acids, and it was associated with higher feed efficiency in calves [29,30,31,32].
Phyla Fibrobacterota and Spirochaetota were declined in Atriplex-fed groups. The members of these phyla are sensitive to tannins [7, 13, 19]. Moreover, these bacteria are involved in the metabolism of complex carbohydrates such as pectin and cellulose and produce acetic acid [6, 33, 34], which is a negative point of feeding on saltbushes.
Rumen methanogens were affiliated mainly with the genus Methanobrevibacter, which declined in AA groups. The decline of the Methanobrevibacter could be attributed to the direct effect of secondary metabolites (tannins, phenols, saponins) that have antimicrobial effects on the methanogens or the protozoa that provide rumen methanogens with hydrogen for methane production [5, 13, 35]. Another explanation for the decline in the rumen methanogens is the low availability of acetate and hydrogen [13, 36]. Previous studies [6, 36] indicated that tannin-rich plants decreased rumen methanogens, methane production, and protozoa count.
The changes in forage type affected the rumen fermentation parameters, due to the changes in the rumen microbial community [5, 13]. The decline in the fiber-degrading and acetate-producing bacteria, such as Fibrobacteres and Sphaerochaeta, might have decreased the fiber digestibility and the acetate production [7, 33, 34], which explains the lower acetic acid in the Atriplex-fed camels [5]. Previous studies on camels [5, 37], sheep and goat [38] reported that the inclusion of halophytes in the diets decreased the cellulolytic enzymes and digestibility. The higher production of propionate, as in the group AA, consumes the hydrogen from the rumen environment, which decreases the availability of hydrogen for methane production, as the hydrogen is the main substrate for rumen methanogens to produce methane [13]. This explanation is supported by lower predicted methane in the AA group. Higher propionic and butyric acids in the AA group could be attributed to the higher butyric and propionic-producing bacteria, such as Prevotella, Anaerovorax, and Moryella, which tolerate the secondary metabolites in Atriplex [13, 25, 27]. Similar findings were obtained in claves supplemented with gallic acid [8]. The total VFA was not affected in camels fed Atriplex, which agrees with previous studies on camels and lambs fed Atriplex and camelthorn [5, 37, 39]. The decline in the rumen ammonia was also reported in camels fed Atriplex [5]. Abdullah et al. [40] noticed a decline in the rumen ammonia in lambs fed Atriplex hay. Lower rumen ammonia could be attributed to the lowered degradation of peptides and deamination of amino acids in the rumen due to the presence of tannins in the Atriplex [4, 5, 39].
Feed intake and growth performance
The values of feed intake were within the ranges indicated in growing camels fed different forages [2, 4]. Including the Atriplex in camel diets did not affect the feed intake. In contrast, previous studies on camels [2, 4] reported increased feed intake when Alfalfa and Rice straw were replaced by Atriplex. Growth performance was slightly declined due to the inclusion of Atriplex in animal diets; however, the values of ADG in the current study were higher than those of camels fed alfalfa hay and Atriplex [2, 4]. In contrast, Farid et al. [2] and Abdel-Wahed [4] reported improved growth rate due to replacing clover hay and rice straw with Atriplex, and they attributed the increase of ADG in camels fed Atriplex to the ad libitum feeding of fresh chopped Atriplex; while Atriplex, in the current study, was offered dried. The decline in growth performance could be attributed to the decrease in digestibility as reported on growing camels fed Atriplex or camelthorn [37, 41]. Similar findings were obtained on sheep and goats fed Atriplex [38, 40]. Furthermore, higher tannins and phenols hinder the absorption of nutrients by animals [42], which justifies the decline in the growth of Atriplex-fed groups, which have approximately similar rumen VFA to group HH fed Alfalfa hay.