Spineless cactus cladode is a viable replacement to barley and maize grains in the feed rations of dromedary camel calves

Abstract Background No studies determined the use of spineless cactus cladodes in camel diets. Objectives The effect of replacing the main energy source in camel diets with fresh spineless cactus cladodes on growth performance was determined. Furthermore, the ability of morphology to predict cladodes yield was determined. Methods A prediction model of spineless cactus cladode weight based on cladode volume was developed. Three cladodes per plants were randomly selected from 100 plants. Weight and volume were then recorded for each cladode. Sixteen male camel calves (196 ± 18.2 kg live weight and 430 ± 5.55 days of age) were allotted to treatments, control (conventional camel fattening diet based on cotton seed hulls, cereal grains and agro‐industrial by‐products) or cactus (barley and maize grains in the control diet were replaced totally by fresh cactus cladode on dry matter basis). The study contained a 100‐days growth trial and a 21‐day digestibility trial (15 days of adaptation and 7 days of faeces collection). Blood samples were collected monthly from each animal. Results Cactus cladode volume predicted the dry weight with a high accuracy (prediction error = 3.5%). Nutrient intake and nutrient digestibility did not significantly differ among the dietary treatments (p > 0.05). The treatment significantly decreased feed conversion ratio by 1.52 points (p < 0.05). All blood parameters were within the normal range of dromedary camels. Conclusions Spineless cactus cladode is a potential replacement to the conventional energy sources in dromedary camel diets.


INTRODUCTION
Camels have an increasingly important role in the livelihood of humans in some geographical regions.The overall population of camels around the world is recently reported as 37,509,000 heads with 27,361,000 heads are kept by the farmers in the arid and semi-arid areas of the developing countries (FAOSTAT, 2019).Previously, camel production was practised within nomadic communities.However, they are now an important component of modern communities in arid regions (Faye, 2016).
The dromedary camel is an excellent source of meat particularly in dry areas where climate negatively impacts the performance of other livestock.This is due to physiological features which enable the dromedary camel to tolerate high temperature, solar radiation, water scarcity and poor nutrition.Camels have relatively low growth rate (500 g/day) (Ali et al., 2019).
To date, grains and grains by-products have been the main energy source of ruminant in the dry areas of the developing countries.However, the decrease in cereal yields as a result of severe drought and global climate change resulted in an increase in the price of cereal grains and their by-products (Ben Salem & Smith, 2008).Therefore, the use of cheaper and more sustainable alternatives is now on the top of priorities of agricultural sectors in developing countries.
Spineless cactus (Opuntia ficus-indica) is a multipurpose plant which is grown by farmers for food production (fruits) and livestock feeding (cladodes).Moreover, it is used to fence farms and homes (Alary et al., 2007).Generally, spineless cactus yields high amount of dry matter ranging from 3.1 to 47.3 t/ha depending on biotic and abiotic factors (Dubeux et al., 2006).Spineless cactus cladode contains high levels of non-structural carbohydrates and calcium (16.5-52.3g/kg) (Heuzé & Tran, 2017).It is highly variable in crude protein (2.6%-11.4%)and neutral detergent fibre (21.4%-37.7%)(Heuzé & Tran, 2017).Supplementation of straw-based diets with spineless cactus cladodes has been shown to enhance nutrient digestibility of sheep (Ben Salem et al., 1996).However, in addition to these favourable attributes, high levels of oxalates have been found in spineless cactus cladodes.Oxalates at a level of 1.1 g/kg live weight in sheep diets have been reported to cause failure in kidney functions, urolithiasis, hypocalcemia and a performance reduction (D'Mello, 1997).More recently, however, it has been established that feeding spineless cactus in combination with fibre-rich feeds tends to alleviate the potential negative consequences associated with oxalates (Ben Salem et al., 2002a).
Determining cactus cladodes yield using a non-destructive method is essential for livestock feeding planning in the farm.Plant morphology has high potential to be used to determine cladode yield in cactus since it showed strong association with forage yield in Atriplex (Ben Salem et al., 2005) and Reed Canarygrass (Casler & Hovin, 1985).
To our knowledge, there is no published data on the effect of spineless cactus cladode on dromedary camel growth performance and health.Furthermore, the ability of morphology to predict cladode yield of spinless cactus is not studied.Therefore, the primary objective of this study is to determine the effect of replacing cereal grains by spineless cactus cladodes on growth performance, nutrient digestibility and health of dromedary camels.In addition to that, the current study aims at determining a simple and robust equation to predict cactus cladodes yield using simple morphology measurements.The remaining concentrate and roughage feeds were collected prior to morning feeding and weighed on daily basis for every camel then stored at −20 • C for feed analyses.Live weight of the experimental camels was measured before morning feeding at day 1 of the trial and every 10 days to obtain weight gain and feed conversion ratio.

Nutrient digestibility
At the last day of the fattening trial, all animals were fitted with faeces collection bags and went through a collection period of 7 days after 14 days of adaptation to faeces bags.Faeces of each camel was collected on daily basis, weighed and subsampled at a rate of 10%.Faces subsamples were oven-dried at 55 • C to reach a constant weight, ground to pass through 1 mm sieve and stored for further analyses.The digestibility (Apparent digestibility of protein) of the experimental diets was calculated from data of the nutrient intakes and the losses in faeces.

Blood sampling and analysis
Blood sampling was done at the start of the trail then monthly.Two blood samples were obtained from each camel through the jugular vein in a heparin tube and an in non-heparin tubes prior to the morning diet.The non-heparin blood tubes were centrifuged (1677 × g; 20 min; 4 • C) then the sera samples were stored at −20 • C for further analyses.Albumin, total protein, glucose, cholesterol, urea, packed cell volume, haemoglobin, alanine transferase, aspartate transferase, creatinine and glutamate oxaloacetate transaminase were determined using specific commercial kits (Katal) and a UV spectrophotometer at the recommended wavelengths.Haemoglobin and packed cell volume were determined using an automated haematology analyser (Diatron, Abacus 5).

Feed and faeces analyses
The feed and faeces samples were dried at 105  (1991) without the use of an alpha amylase.Neutral detergent fibre in this study was presented as residual ash exclusive.Total and soluble oxalates were analysed according to Moir (1953).Total tannins were determined according to Makkar (2003).

Spineless cactus cladodes biomass and morphology data
A total of 100 spineless cactus plants were randomly selected to represent the experimental field and three cladodes were randomly selected from each plant.The longest and shortest diameter, thickness and sundry weight were recorded for each cladode.The cladode surface area (cm 2 ) was calculated as follow: the long diameter (cm) × the short diameter (cm) × π.Cladode volume (cm 3 ) was calculated by multiplying the surface area by the thickness.

Statistical analysis
Blood data and growth performance data were analysed separately.A repeated measurements design was used to analyse blood data with the following specification: where Y is the response variable, TRT is the effect of the treatment, M is the effect of the measurement, Animal is the effect of the camel, TRT × M is the effect of the interaction between treatment and measurement and Ɛ is the residual.
The effect of the treatment on nutrients digestibility and growth performance was analysed according to the following model: where Y is the response variable, TRT is the effect of the treatment and Ɛ is the residual.Fisher's least significant difference at level of 0.05 was used for means separation in both models.
The cladode measurement data was divided into two sets, a calibration set and a validation set using Puchwein (1988) algorithm.The algorithm identified 24 cladodes for the blind validation.Three models were constructed using the calibration set then blindly validated using the validation set.R software version 3.6.1 was used to analysis the study data (R Core Team, 2017).

Spineless cactus cladode biomass prediction
Figure 1 shows that the distribution of spineless cactus cladodes weight and the relation between cactus cladode weight and volume.
The correlation between the cladode weight and morphometry was strong (r > 0.7; p < 0.001) (Table 1).Table 2 presents the performance of prediction models of cactus cladodes weight using cladodes morphology.The three models had similar coefficient of determination (0.854-0.911).Yet, the log-linear model had the lowest 95% percentile prediction error.

Growth performance and blood metabolites
The nutritional composition of the experimental diets is presented in Table 3. Table 4 shows the daily intake of dry matter, organic matter, crude protein as well as the nutrient digestibility of the experimental camels.The experimental treatment did not significantly affect the daily intake of dry matter, organic matter and crude protein of the experimental camels (p > 0.05).The digestibility of dry matter, organic matter, crude protein, neutral detergent fibre, nitrogen free extract and ether extract of cactus group was not significantly different from the control group (p > 0.05).
The feed consumption of the camels was not significantly affected by the treatment (p > 0.05) and nor was the final body weight.The camels fed the cactus diet had significantly (p ≤ 0.05) lower daily growth and feed conversion ratio (by 124 g/day and 1.52 points, respectively) compared to the control (Table 5).
The measurement, animal and the treatment × measurement interaction did not significantly alter blood chemistry parameters of the camels (p > 0.05) (Table 6).The cactus-based diet significantly decreased the albumin, total protein, urea, packed cell volume and haemoglobin of the experimental camels (p < 0.05).Glucose, cholesterol, alanine transferase, aspartate transferase, creatinine and glutamate oxaloacetate transaminase were not significantly affected by the treatment (p > 0.05).

F I G U R E 1
Normal Q-Q plot of cactus cladode weight (g) and its relationship with cladode volume (cm 3 ).

Spineless cactus biomass prediction
A major goal of the current study was to develop a non-destructive method to determine cactus yield of cladodes using cladode morphology.The distribution of cactus cladodes weight was close to normal with some deviation which suggests a log transformation of cladode weight before regressing.The log-linear model had the lowest 95% percentile prediction error.Therefore, this model could be used to predict 95% of cactus cladodes weight using a combination of cladode length, width and thickness with an error less than 3.5%.a Simple linear = Cladode weight (g) = 1.16 + 0.0206 × volume (cm 3 ).
c Quadratic model = Cladode weight (g) = 5.5 + volume(cm 3 ) × 0.0154 mine the amount of cactus cladodes to be included in daily livestock diets.Future studies should continue to develop similar models to predict the nutritive value of cactus cladodes using morphological traits.

Growth performance and blood metabolites
The hypothesis of the current study is that spinless cactus cladodes could be used as the energy source in dromedary camel diets since it is rich in soluble carbohydrates.
The chemical composition of spineless cactus cladodes was within the range reported by Heuzé and Tran (2017).The results of the cur- b Cactus = 2.61 g/kg live weight cotton seed meal + 3.63 g/kg live weight wheat bran + 9.5 g/kg live weight cotton seed hulls + 7.84 g/kg live weight fresh spineless cactus cladodes.
rent study showed that both extract and neutral detergent fibre of spineless cactus cladodes were close to that of barley grains.However, these cladodes had less crude protein compared to barley grains.This is in agreement with Abidi et al. (2009) who also evaluated the nutritive value of cactus cladodes.The current study showed a high content of both total and soluble oxalate in spineless cactus cladodes.Ayadi et al. (2009), Ben Salem and Abidi (2009) and Stintzing and Carle (2005) documented the nutritional composition and anti-nutritional factors of cactus cladodes.The high content of moisture and non-structural (soluble) carbohydrates in spineless cactus cladodes suggests that there a Control = 5.66 g/kg live weight barley grain + 2.18 g/kg live weight maize grain + 2.61 g/kg live weight cotton seed meal + 3.63 g/kg live weight wheat bran + 9.5 g/kg live weight cotton seed hulls.b Cactus = 2.61 g/kg live weight cotton seed meal + 3.63 g/kg live weight wheat bran + 9.5 g/kg live weight cotton seed hulls + 7.84 g/kg live weight fresh spineless cactus cladodes.may be some risk of disturbing rumen fermentation (particularly altering rumen pH) causing acidosis in ruminants.However, the current study indicated that there was no significant difference in nutrients digestibility between cactus and control.This may be due to the protective mechanism induced by the mucilage secretions of spineless cactus cladodes; whereby the mucilage induces more salivation, thus preventing a pH decrease through the buffering effect of increased saliva in the rumen.This is in agreement with Ben Salem et al. (1996) and Tegegne et al. (2007) who also found no adverse effect of spineless cactus cladodes on rumen pH when fed to sheep.Additionally, the presence of pectin in the spineless cactus could be responsible for providing buffering power thus preventing pH reduction (Duskova & Marounek, 2001).
Spineless cactus cladodes have high content of oxalate which could cause damage in rumen wall and the kidney tubules (James, 1978).Yet, camels in both control and cactus groups did not show toxification symptoms and all blood metabolites were within the normal range of healthy camels.This is because the majority of the oxalates in cactus cladodes are insoluble, therefore, they precipitate as insoluble calcium in the rumen (Ben Salem et al., 2002b).Additionally, camels seem to show high oxalates tolerance compared to other livestock species (Dadvar et al., 2019).
In the current study, the digestibility and the organic matter intake and blood glucose were similar between the control and cactus group.
This pinpoints that those camels fed the control and cactus diets received similar amount of energy.Blood albumin and total protein of the experimental camels were decreased due to the dietary treatment.
This indicates to a reduction in protein supply in the small intestine.
In the rumen, pectin is fermented at a faster rate and to greater extent compared to other carbohydrates (Marounek & Dušková, 1999).
Thus, microbial protein synthesis seems to be reduced when feeds rich on pectin (like spinless cactus cladodes and pulps) replaced cereal grains ruminant diets (Balcells et al., 1992) due to the poor synchrony between the supply of energy from cactus and nitrogen from the concentrate.This, together with the lower protein content of cactus cladodes compared to maize and barley grains, could result in a reduction of amino acid flow into the duodenum that would negatively affect animal performance (Beever et al., 1988).This is in agreement with Richardson et al. (2003) and Castrillo et al. (2004) study based on lambs supplemented with barley vs. sugar beet pulp.
The decrease in feed conversion ratio resulted from the dietary treatment in the current study could relate to the increase in feed utilization efficiency or a change in carcass composition, although the latter was not determined in this study.Further studies should deter-mine the effect of spineless cactus cladodes on carcass characteristics and meat quality of camels.
Dromedary camels are kept by the farmers in arid and semiarid areas where there is a limited access to natural pasture and cheap feed.
Yet, integrating spineless cactus, as a source of food and cash in such areas would supply dromedary camels with a cheap energy comparable that of to the traditional energy sources like barley and maize grains.
These expensive grains, replaced by spineless cactus cladodes, would be alternatively used for human consumption and poultry nutrition.
That would improve the overall food security in arid and semiarid areas in the world.
In conclusion, the use of spineless cactus cladodes as energy source in total replacement of maize and barley grains of dromedary camels' diets decreased the feed amount consumed for the production of 1 kg of live weight by 19%.Furthermore, no adverse effect on the health was found on the dromedary camels fed on spineless cactus cladodes in replacement of maize and barley grains.Accordingly, using spinless cactus cladodes as camel feed would decrease the cost of meat production and allow more grains to be used for human and poultry nutrition which would improve the food security of the people in dry areas.
Volume could be used to predict dry weight of spineless cactus cladode using a simple linear model.That model would offer a none-destructive tool to estimate spineless cactus cladode yield.
camels' care and feeding.Hanaa Mfeshi analysed the samples Ashraf Alkhtib and Muhannad Muna wrote the draft.All authors provided advice, revised the progress of the manuscript and approved the final manuscript.
Linear correlation between cactus cladode weight and morphology.
Nutritional composition (g/kg dry matter) of the experimental feedstuffs.Effect of replacing barley and maize grains by spineless cactus cladodes on nutrient intake and digestibility of dromedary camels.
TA B L E 3 a Control = 5.66 g/kg live weight barley grain + 2.18 g/kg live weight maize grain + 2.61 g/kg live weight cotton seed meal + 3.63 g/kg live weight wheat bran + 9.5 g/kg live weight cotton seed hulls.
Effect of replacing barley and maize grains by spineless cactus cladodes on growth performance of dromedary camels.
TA B L E 5 Effect of replacing barley and maize grains by spineless cactus cladodes on blood metabolites of dromedary camels.Control = 5.66 g/kg live weight barley grain + 2.18 g/kg live weight maize grain + 2.61 g/kg live weight cotton seed meal + 3.63 g/kg live weight wheat bran + 9.5 g/kg live weight cotton seed hulls.b Cactus = 2.61 g/kg live weight cotton seed meal + 3.63 g/kg live weight wheat bran + 9.5 g/kg live weight cotton seed hulls + 7.84 g/kg live weight fresh spineless cactus cladodes.
a c T: Effect of dietary treatment; M: effect of measurement; T × M: effect of treatment-measurement interaction.