Effects of replacing alfalfa hay with Atriplex nummularia on the growth performance, digestibility, and energy usage of six-month old camel calves

Abstract

Background

The use of halophytes as fodder, such as Atriplex, is an appropriate strategy for sustainable agriculture and a promising way to fill the gap in the camel feeding in arid and semi-arid areas. This experiment investigated the effects of feeding Atriplex nummularia instead of alfalfa hay on the growth performance, digestibility, and energy utilization in growing camel calves.

Methods

Eighteen six-month-old male camel calves were employed and divided into three groups (n = 6). Animals received a concentrate feed mixture at 0.9% dry matter (DM) of their live body weight (BW) with different roughage sources at 1.1% DM of their BW. The roughages fed consisted of: alfalfa hay alone (T1), a 50:50 mixture of alfalfa hay and Atriplex (T2), or Atriplex alone (T3). During the growing study, animals were weighed once a week, and the proper concentrates and roughages were computed and applied immediately. At the end of the experiment, the digestibility trial, energy measurements, and rumen and blood metabolite analyses were conducted.

Results

Replacing alfalfa hay with Atriplex significantly reduced total organic matter intake and digestibility (P < 0.01), resulting in lower BW changes and average daily gain with a poorer feed conversion ratio. Energy expenditure significantly differed among feeding regimens, with a greater energy balance for those fed alfalfa hay vs. Atriplex. A greater concentration of total protein, globulin, and urea was obtained in camels fed Atriplex (P < 0.05). The inclusion of the Atriplex in the diet decreased serum creatinine, cholesterol, and aspartate aminotransferase (P < 0.05). Replacing alfalfa hay with Atriplex resulted in lower rumen pH (P < 0.01) and higher total volatile fatty acids and ammonia levels (P < 0.05).

Conclusions

In arid environments, Atriplex nummularia can partially or entirely replace alfalfa hay for growing camel calves; however, complete substitution resulted in significant reductions in average daily growth, nutrient digestibility, and feed efficiency. It proposed that Atriplex could be an effective camel fodder for enhancing drought resilience in desert environments.

Introduction

The scarcity of animal feeds is encouraging the use of unconventional feed resources such as halophyte plants in arid and semi-arid regions [1]. These plants are an emerging solution to utilize marginal resources, such as saline soils and water, for providing animal feed [2]. Halophyte crops produce more biomass than traditional forages under saline cultivation conditions [2]. Atriplex has high salt and crude protein content as well as balanced amino acids and moderate crude fiber in comparison to high-quality forages [1, 3]. Halophytes also contain a high concentration of secondary metabolites such as phenols, tannins, flavonoids, and oxalate [4]. The moderate concentration of these metabolites confers beneficial effects as antipathogens, antioxidants, immunological stimulators, and antimicrobials [5]. Furthermore, these compounds protect the protein from rumen degradation while reducing rumen methanogens and methane production [5, 6]. However, excessive concentration of these metabolites reduces the palatability and rumen digestibility [4]. Therefore, raising well-adapted livestock, such as the dromedary camel, to use these halophytes is a viable strategy for sustainable agriculture [7].

Dromedary camels have unique physiological characteristics that enable them to withstand arid climates [8, 9] with high temperatures, poor vegetation, limited feed and water, and secondary metabolites in halophytes [8, 10]. Camels prefer to browse halophytes due to their high moisture and salt content, as they require more salt than other livestock species [11]. Furthermore, camel saliva contains mucin glycoproteins that protect the mucosa of the digestive tract from mechanical damage and prevent the negative effect of plant tannins on protein metabolism in the rumen [7, 11]. These facts explain camels’ high intake of Atriplex [3, 10]. Seasonal feed shortage is the main constraint in camel production, particularly during drought seasons. Therefore, unconventional sources of roughage, such as Atriplex, are being sought to address this issue [3].

The forage quality is one of the main constraints in animal nutrition; therefore, knowledge about forage quality and its interaction with animals’ performance is required to optimize its integration into animal feeding plans [4]. Rabee et al. [7] explained that anti-nutritional factors in saltbushes adversely impact the rumen microbiota and fermentation, which impacts the digestibility and performance. In the same line, Abdel-Wahed [3] reported a drop in the digestibility except for the crude protein in the growing camel calves fed Atriplex compared to clover hay and rice straw. Shawket et al. [11] found that including the Atriplex in camel diets had no effect on the digestibility of dry and organic matter but decreased the crude protein and crude fiber digestibility. Furthermore, including the Atriplex in the diet reduced cellulolytic enzymes, rumen ammonia, and total volatile fatty acids [4, 7]. Growing camels given Atriplex had comparable feed intake, digestibility, and growth performance to those clover hay-fed camels and superior to straw-fed camels [3, 10].

There is less information on incorporating saltbushes into intensive camel farming with its abilities to survive extreme weather conditions at a low feeding cost [12]. Furthermore, this study aimed to investigate the effect of replacing alfalfa hay with Atriplex on feed intake, growth performance, and digestibility in growing camel calves.

Materials and methods

The experiment was carried out in the “National Campaign for the Promotion of Camel Productivity” farm, El-Shalateen Research Station, which belongs to Desert Research Center, Wadi-Hodien, El-Shalatein, Red Sea Governorate, about 1200 km from Cairo, Egypt at 22°00′ 7.20″ N and longitude 36°48′ 9.55″ E. It is an arid region with a desert environment that has almost no precipitation all year long.

Animals and treatments

The current experiment utilized eighteen six-month-old male camel calves, weighing an average of 156 ± 7.81 kg. They were kept in half-shaded, sandy-floor pens with free access to drinking water in half-plastic barrels. The animals were sourced from the “National Campaign for the Promotion of Camel Productivity” farm, which belongs to the Desert Research Center, Egypt. The animals received a concentrate feed mixture (CFM) at 0.9% of their live body weight (BW), with roughage at 1.1% of their BW to cover the nutrient requirements for maintenance and growth [13].

Animals were divided into three groups (n = 6) to be fed one of three roughages: alfalfa hay alone (T1), a 50:50 mixture of alfalfa hay and Atriplex (T2), or Atriplex alone (T3), in which the tender part of the Atriplex nummularia was harvested, sun-dried for 10 days. The CFM and roughage were individually offered twice a day, at 08:00 and 14:00 h. The proximate analysis of CFM, alfalfa hay, and Atriplex nummularia is shown in Table 1. The study lasted for 145 days, including a 45-day adaptation period for feeding Atriplex to growing camels. The growing experiment began immediately after adaptation and lasted for 100 days, in which animals were weighed once a week, and the proper concentrates and roughages were computed based on their new weight and applied immediately. However, the digestibility trial, energy measurements, and rumen and blood metabolite analysis were conducted at the end of the growing experiment.

Table 1.

Chemical composition of concentrate supplement, alfalfa and Atriplex based on a dry matter (DM) basis

Ingredients	*Concentrate feed	Alfalfa	Atriplex
Dry matter, g/ kg fresh matter	943	935	861
Gross energy, MJ/ kg dry matter	14.2	15.9	12.6
Chemical composition, g/ kg DM:
Organic matter	887	881	748
Crude protein	141	127	118
Neutral detergent fiber	387	510	510
Acid detergent fiber	198	398	367

*The concentrate consisted of 55% corn, 15% soybean meal, 10% cottonseed meal, 15% wheat bran, 2.5% limestone, 1.5% salt, 0.5% sodium bicarbonate, 0.1% yeast, 0.1% antitoxins, and 0.3% premix

Digestibility trial

Animals were fitted with fecal bags and given three days to adjust to their new surroundings before collecting feces for the next seven days. They were weighed at the beginning and end of the trial, and the amount of feed intake was recorded daily. Fecal bags were emptied twice a day, and total fecal output was then measured. A 10% subsample was taken and pooled in individual composite samples through the collection period. The samples were dried at 65 °C for 48 h and preserved with feed samples for future analysis. The digestibility was estimated using the acid-insoluble ash corrected for its fecal recovery [14] based on the following equations: (1) The amount of internal marker in feces = The amount of internal marker in intake. (2) Fecal output * %internal marker in feces = Total intake * %internal marker in intake. (3) Fecal output = (Total intake * %internal marker in intake) / %internal marker in feces. (4) Digestibility (%) = (Total intake – Fecal output) * 100/ Total intake. Please note that the total intake equals the sum of the known concentrate and forage intakes.

The rumen fluid and blood samples were collected 2–3 h after the morning feeding. Blood samples were obtained via jugular vein puncture using heparin as the anticoagulant and centrifuged at 10,000×g for 5 min and then stored at − 20 °C for the measurements of the total protein, albumin, urea, creatinine, cholesterol, triglyceride, aspartate aminotransferase (AST), and alanine aminotransferase (ALT) using the laboratory assay kits (Biodiagnostic, Giza, Egypt). Moreover, the rumen liquor samples were withdrawn via a stomach tube [13], and immediately a pH was recorded using a digital pH meter (WPA CD70, ADWA, Szeged, Hungary). Two samples were taken out and then frozen for later determining ammonia [15] and volatile fatty acid (VFA [16]), analysis.

Energy expenditure

Askar [17] and Askar et al. [18] earlier described the calorimetry system and its use in small ruminants and camels, respectively. Experimental animals were outfitted with a face mask that allowed open-circuit respiration for monitoring O₂ consumption. The individual energy expenditure (EE)/heart rate (HR) ratio was determined by taking simultaneous readings from the RCX3 HR (Polar Electro Oy, Kempele, Finland). The concentration of O2 was determined with a fuel cell FC-1B O2 analyzer (Sable Systems, Las Vegas, NV), while EE was estimated by assuming a constant thermal equivalent of 20.47 kJ per liter O2 [19]. Moreover, the HR was thought to be individually collected at 1-minute intervals for at least 24 h, with the daily EE being calculated from the EE: HR ratio for each animal. The Polar software was employed to analyze the collected data.

Weather data

The ambient temperature (T °C) and relative humidity (RH) were measured daily using RC-4HA Temperature and Humidity Data Logger and used to compute the temperature–humidity index (THI) as follows: (0.8 x T) + [(RH/100) x (T − 14.4)] + 46.4 [20].

Chemical analyses

The AIA was used as an internal marker and analyzed according to the method of Van Keulen and Young [21]. Dried samples of feeds and feces were ground and analyzed according to the method of AOAC [15] to measure dry matter (DM), organic matter (OM), and crude protein (CP). Neutral detergent fiber (NDF) and acid detergent fiber (ADF) were measured using ANKOM Technology (ANKOM Technology, New York, United States [22]), . The gross energy (GE) was measured by bomb calorimeter (IKA, model C 200, Staufen, Germany). Metabolizable energy (ME) was considered as 82% of digestible energy (DE) intake.

Statistical analysis

The data was statistically analyzed using the GLM procedure of the SAS statistical package [23]. One-way analyses of variance were employed with feeding treatment as a fixed effect and animal as the random effect. The model was Yij = µ + Ti + eij, where Yij is the dependent variable, µ the overall mean, Ti the fixed treatment effect, and eij is the residual. Differences among means were determined by least significant difference with a protected F-test, and differences with P < 0.05 were accepted as statistically significant.

Results

The mean ambient temperature was 25.4 °C, while those of RH and THI were 56.0 and 72.8%, respectively (Fig. 1).

Fig. 1.

Mean temperature, relative humidity, and temperature–humidity index (THI) throughout the experimental period that growing camel calves were exposed to September–March

Feed intake and growth performance

The average initial BW was similar (P = 0.997) between camel groups (Table 2). Final BW in camel groups fed Atriplex (213 kg, T2 and 205 kg, T3) was numerically lower (P = 0.572) than that of those fed alfalfa hay (229 kg, T1) without a significant difference (Table 2). The average daily gain (ADG) was significantly (P < 0.01) declined by 18 and 29% in calves fed a mix of alfalfa and Atriplex (T2) and those fed Atriplex alone (T3), respectively, compared to animals fed alfalfa hay (T1) (Table 2). Total DM intake was similar among experimental groups. Furthermore, a poorer feed conversion ratio (FCR) was observed with camels fed Atriplex (7.46, T3) compared to those fed alfalfa hay (4.82, T1), while those fed a mix of alfalfa hay and Atriplex (6.34, T2) had an intermediate value (Table 2).

Table 2.

Growth performance of growing camel calves fed Atriplex instead of alfalfa at different levels in the diet

Items	Concentrate feed at 0.9% of body weight
	Alfalfa	Alfalfa/ Atriplex	Atriplex	SEM	P-value
Fattening period, days	100	100	100
Initial body weight, kg	155	155	156	19.6	0.997
Final body weight, kg	229	213	205	20.6	0.572
Body weight changes, kg	74.0a	57.8b	48.4b	3.10	0.000
Average daily gain, g/ day	793a	572b	479c	32.5	0.000
Dry matter intake, g/ day:
Concentrate	1694	1614	1589	172.7	0.847
Hay	2116a	1008b	0.00c	137.3	0.000
Atriplex	0.00c	1008b	1986a	132.2	0.000
Total roughage	2116	2017	1986	215.8	0.847
Total	3810	3631	3575	388.6	0.847
Dry matter intake, g/ kg BW0.75:
Concentrate	32.8	32.2	32.2	0.80	0.713
Hay	41.0a	20.1b	0.00c	0.60	0.000
Atriplex	0.00c	20.1b	40.3a	0.64	0.000
Total roughage	41.0	40.2	40.3	0.99	0.694
Total	73.9	72.4	72.5	1.80	0.698
Feed conversion ratio	4.82b	6.34a	7.46a	0.592	0.005

^{a, b,c} Means having different superscripts within the same row differed significantly (P < 0.05). SEM  Standard error of means

Digestibility of nutrients

Although total DM intake was similar among camel groups, total OM intake was adversely impacted (P < 0.01) when alfalfa hay was replaced with Atriplex, reflecting a significant decrease in the intake of CP and ADF (P < 0.05) (Table 3). Furthermore, camels fed alfalfa hay had higher (P < 0.01) digestibility, whereas those fed Atriplex, either alone (T3) or combined with alfalfa hay (T2), had significantly lower digestibility (Table 3).

Table 3.

Feed intake and digestibility of growing camel calves fed Atriplex instead of alfalfa at different levels in the diet

Items	Concentrate feed at 0.9% of body weight
	Alfalfa	Alfalfa/ Atriplex	Atriplex	SEM	P-value
Body weight, kg	229	194	190	23.1	0.237
Total nutrients intake, g/ day:
Dry matter	4297	3633	3570	431.7	0.237
Organic matter	3798a	3084ab	2894b	374.2	0.086
Crude protein	573	476	458	57.1	0.154
Neutral detergent fiber	1953	1651	1622	196.1	0.237
Acid detergent fiber	1322	1088	1038	131.0	0.124
Total nutrients intake, g/ kg BW0.75:
Dry matter	72.7	69.8	69.8	1.85	0.240
Organic matter	64.3a	59.3b	56.5b	1.60	0.001
Crude protein	9.69a	9.15b	8.94b	0.245	0.033
Neutral detergent fiber	33.0	31.7	31.7	0.84	0.245
Acid detergent fiber	22.4a	20.9b	20.3b	0.56	0.009
Apparent nutrients digestibility:
Dry matter	72.5a	69.4b	64.0c	0.60	0.000
Organic matter	77.8a	75.3b	69.9c	0.54	0.000
Crude protein	71.6a	67.0b	60.3c	1.20	0.000
Neutral detergent fiber	61.0a	57.3b	49.0c	1.37	0.000
Acid detergent fiber	52.8a	47.4b	37.9c	1.54	0.000

^{a, b, c} Means without a common superscript letter in the row are differed (P < 0.05) between treatments. SEM  Standard error of means

Energy utilization

The effects of replacing alfalfa hay with Atriplex on energy utilization are shown in Table 4. In line with OM intake and digestibility, increasing Atriplex in the diet reduced GE and DE (kJ/kg BW^0.75) intakes. A higher DE (P < 0.01, %) was observed for those fed alfalfa hay vs. Atriplex, while those fed mixed roughage had an intermediate value. The ME followed the same pattern as the DE. However, HR (beats/min) significantly differed among treatments. Replacing alfalfa hay with Atriplex had a significant negative effect (P < 0.01) on EE, which was greatest for camel calves fed alfalfa and lowest for those fed Atriplex. This, together with higher ME intake, resulted in a greater energy balance for calves fed alfalfa hay vs. Atriplex as the sole forage.

Table 4.

Energy utilization of growing camel calves fed Atriplex instead of alfalfa at different levels in the diet

Items	Concentrate feed at 0.9% of body weight
	Alfalfa	Alfalfa/ Atriplex	Atriplex	SEM	P-value
Energy utilization:
Gross energy, kJ/ kg BW0.75	1100.5a	996.9b	929.8c	27.17	0.0001
Digestible energy, kJ/ kg BW0.75	813.5a	685.5b	577.4c	21.02	0.0000
Digestible energy, %	73.9a	68.9b	62.2c	0.86	0.0000
Metabolizable energy, kJ/ kg BW0.75	667.1a	562.1b	473.4c	17.24	0.0000
Heart rate, beat/ min	65.7a	56.2b	52.1c	1.06	0.0000
Energy expenditure, kJ/ kg BW0.75	433.5a	371.1b	344.1c	6.98	0.0000
Energy balance, kJ/ kg BW0.75	233.6a	191.0b	129.4c	17.46	0.0003

^{a, b, c} Means without a common superscript letter in the row are differed (P < 0.05). SEM  Standard error of means

Blood and rumen metabolites

The effects of replacing alfalfa hay with Atriplex on some blood and rumen metabolites are shown (Table 5). A greater concentration of total protein, globulin, and urea was obtained in camels fed Atriplex (P < 0.05). Atriplex feeding decreased serum creatinine, cholesterol, and AST (P < 0.05). However, replacing alfalfa hay with Atriplex decreased rumen pH (P < 0.01) and increased total VFA and ammonia (P < 0.05) (Table 5).

Table 5.

Blood and rumen metabolites of growing camel calves fed Atriplex instead of alfalfa at different levels in the diet

Items	Concentrate feed at 0.9% of body weight
	Alfalfa	Alfalfa/ Atriplex	Atriplex	SEM	P-value
Blood parameters:
Total protein, g/ dl	5.46b	5.20b	5.91a	0.193	0.009
Albumin, g/ dl	3.66	3.40	3.39	0.183	0.337
Globulin, g/ dl	1.81b	1.82b	2.51a	0.155	0.001
Cholesterol, mg/ dl	125	114	110	10.0	0.373
Triglyceride, mg/ dl	83.2b	85.9ab	89.2a	2.59	0.148
Urea, mg/ dl	4.03b	4.67a	4.51a	0.202	0.028
Creatinine, mg/ dl	1.84a	1.67b	1.39c	0.046	0.000
AST, IU/ dl	103ab	108a	96b	4.2	0.051
ALT, IU / dl	42.2	42.4	42.7	0.29	0.322
Rumen parameters:
pH	6.77a	6.29b	5.83c	0.077	0.000
Ammonia, mg/dl	9.8b	14.7a	15.8a	1.61	0.032
Volatile fatty acids, m.eq/ dl	6.48b	9.93a	12.6a	1.29	0.007

^{a, b, c} Means without a common superscript letter in the row are differed (P < 0.05). SEM  Standard error of means

Discussion

The limited availability of natural resources highlights the camel as an integral animal in sustainable agriculture because of its ability to convert halophytes, which other domestic animals do not prefer, into animal products [2, 7]. Halophytes chemical composition limits their palatability and ingestion [24]. The results obtained for the chemical composition indicated that Atriplex has lower OM and CP and similar fiber fraction contents compared to alfalfa, which is similar to that reported by Farid et al. [10], while that of alfalfa hay is within the range indicated by Askar et al. [18]. However, Atriplex contains several secondary metabolites, such as phenols, tannins, flavonoids, saponins, oxalates, alkaloids, and resins [7].

Digestibility and performance

The secondary metabolites in halophytes affect rumen microbial population, digestibility, and performance [7, 12], which might explain the lower nutrients digestibility and lower ADG in calves fed Atriplex (T2 and T3) compared to those fed alfalfa hay (T1). Abdel-Wahed [3] reached a similar conclusion, reporting declines in nutrient digestibility with the exception of CP digestibility, which improved when alfalfa was replaced by Atriplex. Shawket et al. [11] found decreased digestibility of CP, CF, and fat in camels fed Atriplex. Askar et al. [25] reported a drop in digestibility when sheep and goats were fed Atriplex instead of alfalfa hay. Dadvar et al. [4] concluded that antinutritional factors in Atriplex negatively affected the rumen microorganisms. Rabee et al. [7] reached similar findings and reported that tannins inhibited camel rumen cellulolytic bacteria such as Fibrobacteres, which negatively impacted DM and NDF digestibility in the rumen. These findings are supported by a reduction in cellulolytic enzymes in camels fed Atriplex [4].

The reduction in digestibility caused by replacing alfalfa hay with Atriplex was associated with a decrease in ADG (T2 and T3). This decline in growth rate as a result of feeding Atriplex was also reported in lambs when wheat straw was completely replaced by Atriplex [26]. In contrast, Farid et al. [10] and Abdel-Wahed [3] found that substituting Atriplex for clover hay and rice straw improved the ADG of camel calves, which could be attributed to the ad libitum feeding of fresh chopped Atriplex compared to restricted dried crushed Atriplex (1.1% of BW, Tables 2 and 3). Shawket et al. [11] indicated that digestibility and growth rate were improved in camels fed Atriplex when the feeding period was prolonged from 180 to 360 days, which might be attributed to the adaptation of rumen microorganisms to the antinutritional factors [10, 11], highlighting the camel as a well-adapted animal to feed on halophytes. However, the growth rate in the current study (Table 2) was greater than that of camel calves fed alfalfa hay or Atriplex [3, 10, 11], most likely due to the sex, age, or initial BW of the camel calves [13]. Also, the breed may be involved [27, 28], as this growth rate was greater than that of camel calves fed alfalfa or Alhagi maurorum [12], with higher DM intake than in the current study. However, the inclusion of the Atriplex did not impact the feed intake (g/kg BW^0.75, Tables 2 and 3), which was within the normal range of camel calves fed different forages [3, 10, 11, 13, 18]. Previous studies on camel calves [3, 10] reported that including the Atriplex in camel diets increased the feed intake compared to camels fed alfalfa hay.

Rumen fermentation and blood metabolites

The replacement of alfalfa hay with Atriplex increased rumen ammonia, resulting in greater total protein and urea levels in blood. In contrast, Abdullah et al. [26] observed a decrease in rumen ammonia in lambs fed Atriplex, which was similar with the findings of Dadvar et al. [4] in camels. They attributed the decreased ammonia to the lower nitrogen degradation in the rumen due to the presence of tannins in the Atriplex [3, 4]. However, camel calves, in the current study, were fed concentrate first, followed by Atriplex, which was fed at a slower rate than alfalfa hay. This concentrate feed consisted of 14.1% CP, including different sources of protein with a considerable amount of degradable nitrogen, which probably contributed to the elevated ammonia levels in the rumen. Rabee et al. [29] recently reported a significant decline in rumen ammonia in camel calves fed Atriplex rather than alfalfa hay for 6 months longer than those in the current experiment, highlighting the camel’s adaptation to feeding on halophytes with a similar rate to alfalfa hay. Shawket et al. [11] found that feeding Atriplex for 12 months rather than 6 months enhanced camel calves’ digestibility and growth rate, which was attributed to the rumen microorganisms adapting to Atriplex’s antinutritional factors. On the other hand, a higher VFA when alfalfa hay was replaced with Atriplex coincided with a lower rumen pH. A considerable amount of non-structural carbohydrates in the concentrate feed with 55% corn was probably the main reason for the lower pH and higher VFA when Atriplex was fed instead of alfalfa (T2 and T3). Abdullah et al. [26] noticed an increase in rumen VFA in lambs fed Atriplex. However, higher rumen concentrations would certainly meet the requirements for microbial synthesis [30], implying higher nitrogen degradation in conditions of high fermentable energy availability (higher VFA), which would enhance microbial protein synthesis, nutrient utilization (Table 3), and, as a result, camels’ performance (Table 2). In contrast, total VFA numerically decreased in camels fed Atriplex, as previously noted in growing camels fed Atriplex or camelthorn [4, 12]. Similarly, Ahmed et al. [6] found a decline in rumen VFA in lambs fed Atriplex, which could be attributable to diluted ruminal content due to increased water consumption when animals were fed saltbushes, but this was not relevant to the current study with camel calves. Rabee et al. [29] recently reported that feeding Atriplex to camel calves for an extended period of time resulted in a similar total VFA.

The blood metabolites were within the normal range for growing camels [12, 13, 31], but differed from those reported by Faraz [32] and Faraz et al. [33], implying that breed or age may be a factor. The replacement of alfalfa with Atriplex increased blood total protein, which is consistent with the findings in lambs fed Atriplex [6]. Furthermore, a higher blood urea was observed when Atriplex rather than alfalfa hay was fed. The findings were in line with Dadvar et al. [4] and could be attributable to increased ammonia and its absorption through the rumen wall [4, 6]. However, the decline in blood cholesterol and liver enzymes (AST) was linked to a lower rumen pH, and also reported in camel calves after replacing alfalfa with Alhagi maurorum [12]. Ahmed et al. [6] reported a decline in blood cholesterol and an increase in blood urea in lambs fed Atriplex. Ghavipanje et al. [12] reported that active compounds in the halophytes, such as flavonoids and phenols, decrease blood cholesterol, liver enzymes, triglycerides, and oxidative stress. Ahmed et al. [6] explained that tannins in the Atriplex form a complex with fatty acids, which decreases the absorption of cholesterol and increases the fat excretion. The decline in the liver enzymes indicated normal liver function in camels fed Atriplex [6, 12].

Energy utilization

The relationship between EE and ME intake revealed that Atriplex had significantly higher EE than alfalfa hay (EE = 73 vs. 65% of ME intake, respectively), which could be explained in part by the effects of the forage quality on gut mass and energy use [25]. It is expected that Atriplex, as a low-quality forage, requires more energy for digestion than alfalfa hay, which is a high-quality forage; this difference is likely to contribute to the variation in EE between the two forage types. This, together with the lower ME intake for Atriplex vs. alfalfa hay, was reflected in the energy balance, which was greater for those fed alfalfa hay vs. Atriplex, while the mixed forage treatment had an intermediate value (Table 4), consistent with the lower ADG for Atriplex vs. alfalfa hay (Table 2). Similar findings were observed with sheep and goats when they were fed Atriplex nummularia compared to alfalfa hay [17]. Forage quality has been reported to affect EE and requirements in livestock species [34, 35]. Although Atriplex contains various secondary metabolites that reduce its quality [7] and affect its EE, it has a positive energy balance with a moderate digestible energy (62.2%, Table 4) and moderate ADG (480 g/day, Table 2). This is considered a positive result with feeding Atriplex, although camel calves fed alfalfa hay performed better (Table 2).

Halophytic plants were reported to have varied degrees of digestion and use among animal species. Small ruminants fed on Atriplex cannot sustain their live BW [36–38]. Sheep and goats fed Atriplex nummularia [39] or Acacia saligna [40] had a negative impact on feed intake with a negative energy balance, but those fed alfalfa hay had a positive balance. However, the energy supplement (concentrate feed, Table 1) might have great importance in improving performance when Atriplex was fed. Atriplex could prove to be a good and cheap source of nitrogen [17, 41, 42] in the presence of energy sources. Ben Salem et al. [38] reported that Atriplex is deficient in energy and has approximately 65% of nitrogen as non-protein nitrogen. In the current study, replacing Atriplex with alfalfa did not affect the forage or the total intake (Tables 2 and 3), with a positive energy balance (Table 4) and moderate or good performance (Table 2). Camels can handle high salt levels and adapt to water scarcity and oxalate because of efficient kidney and rumen adaptations, while small ruminants are more sensitive to high ash/salt loads [25, 40, 43], and their intake is limited by high salt and secondary compounds [25, 44]. Excessive intake of Atriplex with high salt levels in small ruminants may reduce palatability and overall consumption, potentially leading to the risk of oxalate poisoning or digestive disturbance [41, 43]. Water requirements increase when feeding Atriplex, as animals need to excrete salts; however, camels can tolerate long intervals without water [13], while small ruminants require frequent access to water when fed Atriplex due to increased water demand [41].

Generally, feeding Atriplex to camels is safe, although excessive amounts may soften feces [44] as a result of consuming a large amount of water. Atriplex is more palatable and preferred by camels due to their high moisture and electrolyte content [10, 45, 46]. On the one hand, it may be related to their greater need for salt than other animal species, which is in higher proportion in the Atriplex. Camels require six to eight times as much salt as other animals [47, 48], with camels without regular access to salty feed requiring approximately 140 g of salt per day [49]. On the other hand, camel saliva contains varying amounts of high molecular weight mucin glycoprotein, which protects the mucosa of the digestive tract from mechanical injuries and fixes plant tannins, preventing their negative effects on protein metabolism in the rumen [50]. It is concluded that Atriplex is considered a strategic forage for enhancing drought resilience; it can be efficiently utilized by camels, supporting maintenance and moderate production, and serves as a valuable source of protein and mineral supplements [44].

Conclusion

In arid regions where cattle cannot be raised, Atriplex nummularia can partially or entirely replace alfalfa hay for growing camel calves; however, complete substitution resulted in significant reductions in average daily growth, nutrient digestibility, and feed efficiency. It suggested that Atriplex could be an effective camel fodder for enhancing drought resilience in desert environments.

Abbreviations

DM

Dry matter

BW

Body weight

CFM

Concentrate feed mixture

AST

Aspartate Aminotransferase

ALT

Alanine Aminotransferase

VFA

Volatile fatty acids

HR

Heart rate

EE

Energy expenditure

RH

Relative humidity

T

Ambient temperature

THI

Temperature–humidity index

OM

Organic matter

CP

Crude protein

NDF

Neutral detergent fiber

ADF

Acid detergent fiber

SEM

Standard error of means

ADG

Average daily gain

FCR

Feed conversion ratio

GE

Gross energy

DE

Digestible energy

ME

Metabolizable energy

Authors’ contributions

Formal analysis: A.R.A., A.A.A., G.A.B. Investigation: A.R.A., A.A.A., G.A.B., O.R., E.M.G., F.F. E.S., H.H.A., S.S. S.S.A., M.M.S., A.E.R. Methodology: A.R.A., R.D., A.A.A., G.A.B. Writing-original draft preparation: A.R.A., A.E.R. Writing-review, and editing: A.R.A., G.A.B., M.M.S., A.E.R., U.A.N., H.M.K., Validation and supervision: A.R.A., G.A.B., E.M.G. All authors read and approved the final manuscript.

Funding

This research work was funded by the Academy of Scientific Research and Technology (ASRT), Egypt, through the National Project “The National Campaign for the Promotion of Camel Productivity”, Principal investigator: Prof. Ahmed Askar. The Science, Technology, and Innovation Funding Authority (STDF) provides open access funding in collaboration with the Egyptian Knowledge Bank (EKB).

Data availability

All data and materials are owned by the authors and/or no permissions are required.

Declarations

Ethics approval and consent to participate

This study was carried out in accordance with the Local Experimental Animal Care and Welfare Committee and approved by the Institutional Ethics Committee affiliated with the Animal and Poultry Production Division, Desert Research Center, Egypt (Approval No. 1952021). All methods and protocols adhered to the Universal Directive for the Protection of Animals Used for Scientific Purposes. All protocols follow the ARRIVE guidelines for reporting animal research (https://arriveguidelines.org).

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.