Influence of season and rangeland-type on serum biochemistry of indigenous Zulu sheep

1 Introduction

Indigenous Zulu sheep are slow-growing, small to medium body size with either fat carrot-shaped or thin tail [1]. Zulu sheep, which are commonly found in KwaZulu-Natal province of South Africa, have multi-colored coat with tangled fur. These Nguni sheep have distinctive black, brown, dark brown, or white fur and small ears [2]. Keeping Zulu sheep is the mainstay of the rural economy and food security to resource-limited farmers because of their unique adaptability traits. Zulu sheep have the ability to endure dry conditions [1]. Various adaptability traits of Zulu sheep include resistance to ticks and tick-borne diseases and parasites infestation and aptitude to produce and reproduce under the hot dry and humid climatic conditions [1,2]. In addition, Zulu sheep are able to walk long distances in search of food and water [3]. Nonetheless, the major threat to the existence of Zulu sheep is indiscriminate crossbreeding under extensive production system by rural farmers who desire rapid growth rates and production of large-framed carcasses [4]. As a result, Zulu sheep are prone to extinction.

The Department of Agriculture, Forestry, and Fisheries in collaboration with the Agricultural Research Council have established a programme called the Animal Genetic Resource, which aims to conserve and develop indigenous livestock through traditional conservation approaches and modern biotechnological techniques. Zulu sheep have been identified as an indigenous and endangered breed that require conservation in their environment. To strengthen their in situ conservation schemes, status of biochemical profile is among factors that need to be understood. The Zulu sheep are normally raised on communal rangelands [3,5] where there is an inconsistent availability of herbaceous biomass and quality. Grazing rangelands are continually changing ecosystem because of complex interactions between plants, water, nutrients, and livestock [6]. Availability and quality of forage vary seasonally because of temporal fluctuations in temperature and moisture availability [7]. The quantity and quality of forages during dry season is the main constraint resulting in reduced productivity in communal rangeland [6]. The availability and quality of forage is low particularly in dry season [5]. Variations in quantity and quality on rangelands have direct bearing on biochemical profile of Zulu sheep. Before introducing any feeding strategies to improve Zulu sheep performance, determination of biochemical profile of Zulu sheep in a given rangeland across seasons is pertinent.

The availability of woody and herbaceous species, forage availability, and availability of nutritious alternative feedstuffs are among factors influencing sheep performance [8]. These factors could have a direct effect on nutritional and health statuses of sheep. Determining blood bio of nutritionally related blood metabolites increases understanding of the adaptability of Zulu sheep to production conditions and helps to formulate ways to improve their production [9]. Information on the blood metabolite profile of Zulu sheep is scarce. It is, therefore, crucial to assess the nutrition-related blood metabolites of Zulu sheep raised in different rangelands to establish a reference value for assessing their nutritional status. Understanding nutritional status of Zulu sheep in different seasons and rangeland types will assist sheep farmers by predicting where and when should they provide supplementary feeding. Determining serum biochemistry increases understanding of the adaptability of Zulu sheep to production conditions and helps to formulate ways to improve their production. The blood plays an important role in transporting nutrients to cells and performing functions such as regulatory, protective, and homeostatic functions in mammals [9]. Serum biochemistry can be used to explain the quality of forage grazed by animals. It can also be used to measure metabolic state of Zulu sheep because they are the main indices of physiological and nutritional status of animals. Thus, serum biochemistry may have a direct bearing on nutritional and health statuses of Zulu sheep. The objectives of the study were to determine serum biochemistry of Zulu sheep raised in different types of rangelands across seasons. It was hypothesized that serum biochemistry of Zulu sheep is influenced by season, rangeland type, and their interaction.

2 Materials and method

3 Results

3.1 Effect of rangeland type on body weight and blood metabolites

The effect of rangeland type on body weight and body condition score is shown in Figure 1. Sheep with highest body weights were observed in LV and NSS (P < 0.05). Sheep with highest body condition score were found in MCT, LV, and DHS (P < 0.05). Effect of rangeland-type on blood metabolites of Zulu sheep is displayed in Table 2. The concentration of albumin was high (P < 0.05) in MZT and DHS and low (P < 0.05) in NSS. Globulin and total protein concentrations were high (P < 0.05) in the NSS. Sheep with high levels of glucose were found in DHS (P < 0.05). Sheep with high levels of non-esterified fatty acids were found in DHS, NSS, and MCT (P < 0.05). Cholesterol levels were low in LV (P < 0.05). Blood urea nitrogen (BUN) was high in DHS and NSS. The levels of β-hydroxyl-butyrate were low (P < 0.05) in DHS.

Figure 1

Effect of rangeland type on body weight and body condition score of Zulu sheep. LV – Lowveld; MZT – Moist Zululand thornveld; DHS – Dry Highland Sourveld; NSS – Natal Sour Sandveld; CFT – Moist Coastal Forest and Thornveld; SEM – standard error mean.

Table 2

Effect of rangeland type on blood metabolites of Zulu sheep

Variable	Rangeland type					SEM	P-value
	LV	MZT	DHS	NSS	MCFT
Albumin (g/L)	21.8b	24.7c	25.1c	16.4a	22.6bc	0.512	<0.001
Globulin (g/L)	55.5b	43.2a	45.6a	68.1c	44.4a	1.344	<0.001
Total protein (g/L)	77.4b	68.1a	69.7a	84.5c	66.9a	1.457	<0.000
Creatinine (µmol/L)	59.8	60.9	59.5	60.7	60.2	1.677	0.066
Glucose (mmol/L)	3.07a	3.27a	3.77c	3.29ab	3.48b	0.102	<0.001
Non-esterified fatty acids (mmol/L)	0.44a	0.38a	0.55b	0.51b	0.63b	0.041	0.001
Cholesterol (mmol/L)	1.44a	1.59b	1.61b	1.58b	1.78c	0.056	<0.001
Blood urea nitrogen (µmol/L)	5.89a	5.83a	6.61b	6.66b	5.85a	0.162	<0.001
β-Hydroxyl-butyrate (mmol/L)	0.40b	0.48bc	0.29a	0.38b	0.58c	0.025	<0.001

LV – Lowveld; MZT – Moist Zululand Thornveld; DHS – Dry Highland Sourveld; NSS – Natal Sour Sandveld; CFT – Moist Coastal Forest and Thornveld; SEM – standard error mean. Values in the same row with different superscript letters differ (P < 0.0.5).

3.2 Effect of season on body weight and blood metabolites

Influence of season on body condition score and body weight is shown in Figure 2. Body condition score and body weight were higher in rainy season than dry season (P < 0.05). As displayed in Table 3, albumin, total protein, and creatinine levels were higher in dry season (P < 0.05). Glucose and BUN were higher in rainy season (P < 0.05). Non-esterified fatty acid was not influenced by seasons.

Figure 2

Effect of season on body weight and body condition score of Zulu sheep.

Table 3

Effect of season on nutrition-related blood metabolites on Zulu sheep

Variable	Season		SEM	P-value
	Dry	Rainy
Albumin (g/L)	23.4	20.9	0.322	<0.001
Globulin (g/L)	52.1	50.6	0.850	0.209
Total protein (g/L)	75.5	71.1	0.921	0.001
Creatinine (µmol/L)	63.5	56.4	1.055	<0.001
Glucose (mmol/L)	3.27	3.48	0.065	0.019
Non-Esterified fatty acids (mmol/L)	0.53	0.48	0.025	0.132
Cholesterol (mmol/L)	1.57	1.63	0.036	0.238
Blood urea nitrogen (µmol/L)	5.66	6.66	0.102	<0.001
β-Hydroxyl-butyrate (mmol/L)	0.42	0.43	0.016	0.437

SEM – standard error mean.

Table 4

Correlation between body weight and serum metabolite concentrations in Zulu sheep

	BW (kg)	TP (g/L)	ALB (g/L)	CTN (µmol/L)	GLU (mmol/L)	NEFAs (mmol/L)	CHOL (mmol/L)	BUN (µmol/L)	BHB (mmol/L)	GLOB (g/L)
BW (kg)
TP (g/L)	0.242**
ALB (g/L)	0.010ns	0.150*
CTN (µmol/L)	0.258**	0.119ns	–0.029ns
Glu (mmol/L)	–0.125ns	–0.163*	0.074ns	–0.071ns
NEFAs (mmol/L)	–0.042ns	0.083ns	0.052ns	0.019ns	0.016ns
CHOL (mmol/L)	–0.050ns	–0.018ns	0.240**	–0.045ns	0.068ns	0.223**
BUN (µmol/L)	0.059ns	–0.003ns	–0.171*	–0.055ns	0.168*	–0.007ns	0.061ns
BHB (mmol/L)	–0.182**	–0.112ns	–0.135ns	–0.018ns	–0.059ns	0.121ns	–0.014ns	–0.065ns
GLOB (g/L)	0.206**	0.919**	–0.484**	0.061ns	–0.146*	0.045ns	–0.124ns	0.064ns	–0.052ns

ns – Not Significant; **P < 0.01; *P < 0.05; BW – Body weight; TP – Total protein; ALB – Albumin; CTN – Creatinine; GLOB – Globulin; BUN – Blood Urea Nitrogen; GLU – Glucose; CHOL – Cholesterol; NEFAs – Non-Esterified Fatty Acids; BHB – β-hydroxyl-butyrate.

3.3 Interaction between season and rangeland type on serum biochemistry

There was a significant interaction between season and rangeland type (P < 0.05). Interaction between season and rangeland type on serum biochemistry is shown in Figures 3 and 4. In LV, albumin concentration was high in rainy season than dry season (P < 0.05). In NS, albumin concentration was high in dry season than in rainy season (P < 0.05). Globulin concentration was higher during dry season in MCT (P < 0.05). In MCT, there was a higher total protein concentration in dry season than in rainy season (P < 0.05). In LV, cholesterol was high in rainy season compared to dry season whereas in the NSS, the inverse was observed (P < 0.05). In MZT, there was high concentration of non-esterified fatty acids during rainy season, while in the NSS, non-esterified fatty acids were high in dry season (P < 0.05).

Figure 3

Interaction between season and rangeland type on serum biochemistry of Zulu sheep. LV – Lowveld; MZT – Moist Zululand Thornveld; DHS – Dry High Sourveld; NSS – Natal Sour Sandveld; CFT – Moist Coastal Forest and Thornveld; SEM – standard error mean.

Figure 4

Interaction between season and rangeland type on serum biochemistry of Zulu sheep. Lowd – Lowveld; MZT – Moist Zululand thornveld; DHS – Dry High Sourveld; NSS – Natal Sour Sandveld; CFT – Moist Coastal Forest and Thornveld; SEM – standard error mean.

In LV, higher glucose concentration was observed in rainy season compared to dry season whereas in MCT, the contrary was noted (P < 0.05). In LV, levels of BUN were higher in rainy season than in dry season (P < 0.05). In DHS, similar levels of BUN were observed in both seasons. In LV, β-hydroxyl-butyrate concentration was higher during the dry season compared to rainy season (P < 0.05). In NSS, the concentration of β-hydroxyl-butyrate was significantly higher in rainy season compared to dry season. Creatinine concentration was significantly high during dry season in LV, NSS, and MCT.

4 Discussion

Body weight and body condition score are used to measure the nutritional status of animals; however, due to their shortfalls in remote areas, such methods can be coupled with measurements of serum biochemistry profiles. The abundant vegetation such as Acacia karroo, A. nigrescens, A. nilotica, A. robusta, A. tortilis, A. xanthophloea, Berchemia zeyheri, Combretum apiculatum, and Eragrostis gummiflua in the Natal Sourveld could influence the observation that Zulu sheep grazing in LV and Natal Sourveld had the highest body weights. For example, Acacia species are a valuable feed resource widely used in the semi-arid areas of Southern Africa, particularly during the dry season [14]. Leaves from Acacia species contain high nutrient contents, including crude protein and essential amino acids which could have caused improvement in body weights. The general increase in sheep body weight could have resulted in increased body condition owing to high nutritive forage quality during the rainy season. Herbaceous plant species consumed during the rainy season are usually succulent and nutritious due to showers of rain [15], which causes re growth of vegetation. Seasonal variations across the year have a huge influence on the mineral concentration of the grass and alternatively on blood serum concentrations [16].

Albumin, a protein produced by the liver, is responsible for modulating fluid from leaking out of blood vessels, and nourishes tissues, and transports hormones, vitamins, drugs, and substances throughout the body. High levels of albumin concentration could mean that factors such as physiological and hormonal status were more sensitive and specific than a change in nutritional status. Palatability and toxicity of consumed forage may also lead to high albumin. In the present study, the palatability and toxicity analyses were not measured. The observed higher levels of serum albumin in Zululand Thornveld and DHT contradict results reported by Pelve et al. [17]. The differences could mainly be attributed to different vegetation type. Higher body weight and body condition score observed during the rainy season compared to dry season were anticipated because of high availability of forage from the pasture [14]. The observed changes in body weight, however, contradict findings by Kunene and Fossey [2] and Nyamukanza et al. [5] who reported that weights of Nguni sheep were less affected by season. This result could be due to extended period of drought observed in KZN between 2014–2015 that had resulted in some rangeland vegetation with low nutrients and carrying capacity for grazing. In addition, it was observed that some areas were having minimal or no access to water (rivers) for animals to drink. However, this research did not focus on evaluating the sources of drinking water on animal production. Globulins are part of the globular proteins that possess higher molecular weights than albumin. Globulin is abundantly found in plants, where it functions as protein storage [5]. The observed higher globulin concentration during the dry season in MCT rangeland type could indicate that Zulu sheep are hardy and resistant to disease and parasites [5]. It is possible that the change in blood globulin concentration is also related to the immune and health status of the animal. High globulin concentration during the dry season in MCT rangeland type corroborates the findings of high total protein concentration in the said season in MCT, respectively.

Total protein is comprised of both albumin and globulin meaning that sheep grazing from the in MCT were able to increase their protein status from the consumed forage [18]. Increase in total protein concentration could be reflected by sensitivity and specificity of hormonal balance, nutritional status, water balance, and state of health. Findings that cholesterol in LV rangeland was higher in rainy season resonate with Nyamukanza et al. [5] and Mapiye et al. [19]. It is also possible that during the dry season there was high level of heat loss from sheep and energy imbalance because of severe cold associated with the season, which could have led to sheep suffering from cold stress as they graze [20]. Hence, the lower cholesterol level during the dry season could be due to poor thermogenesis caused by failure of sheep to adapt to cold environment.

Non-esterified fatty acids (NEFAs) are a product of hydrolysis of triglycerides stored in adipose tissue that can be used as an energy source by several tissues in the body [21]. In ruminants, NEFA reflects triglyceride metabolism and fluctuates during starvation and poor feed supply due to energy-demand-induced lipolysis. The observation that in MZT, NEFAs were high during rainy season could be a reflection that Zulu sheep have high energy requirement; therefore, high energy demands and high amount of adipose tissue breakdown. In NSS, high levels of NEFA could be due to low levels of rainfall and poor quality of forage. Therefore, sheep tends to struggle to meet their energy demand, thus leading to depleted body reserves. An increased physical activity in search of food may also contribute to high levels of NEFA [19]. Physiological response to nutritional stress is expressed as a mobilization of lipids from body fat to meet energy demands. Grass species found in the NSS such as Eragrostis gummiflua and Monocymbium ceresiiforme are categorized as very hardy, perennial grass with sparse, hard, and tough leaves. As such, this could have made it hard for sheep to properly digest and utilize them [22]. The lower glucose concentration in the LV rangeland during dry season could be due to energy restriction suggesting that the plane of nutrition was inadequate to satisfy glucose requirements.

Glucose demonstrates the efficiency of energy utilization in a given food [18], as such high glucose during rainy season in LV rangeland suggest that sheep were able to maintain blood glucose homeostasis. High glucose concentration could also be related to high rainfall and feed availability [19]. The high glucose concentration in the DHS could be due to levels of glucose found in pennisetum clandestinum, a dominant grass in the said rangeland type [23]. Blood glucose could also be affected by secondary metabolites of plants in a particular rangeland. However, metabolites were not measured in the present study. BUN is positively associated with crude protein intake and fraction of rumen degradable protein and rumen undegradable protein when forage containing sufficient energy are fed [18]. High BUN in the rainy season suggests that body protein reserves were catabolized to support glucose synthesis. Similar BUN in the DHS in both seasons could suggest failure of sheep to catabolize adipose body tissue reserves. There is also a need to determine the crude protein concentration of the rangeland plants and their rumen degradable protein concentration, which may have affected the rumen ammonia and thus blood urea. Although the findings that β-hydroxyl-butyrate concentration was higher during the dry season in LV and higher in the NSS in the rainy season are difficult to clarify. However, assuming that β-hydroxyl-butyrate concentration was affected by unknown factors, it appears that sheep were able to meet the nutritional requirements throughout the duration of the study. The observation that creatinine concentration was high during dry season in LV, NSS, and MCT disagrees with Nyamukanza et al. [5]

The observed positive correlation between NEFA and cholesterol concentration is complex to explain. A negative correlation was expected because of high glucose concentration that propels more insulin to be secreted [24]. High insulin causes a reduction in blood NEFA. Insulin inhibits breakdown of fat in adipose tissue by inhibiting the intracellular lipase that hydrolyzes triglycerides to release fatty acids. Perhaps high insulin, due to high glucose concentration, caused a decline in cyclic adenosine monophosphate concentrations, thus stimulating cholesterol synthesis. Total protein has, if any, little effect on glucose concentration. Hence, the negative correlation between total protein and glucose concentration is difficult to explain. It is, however, safe to assume that during the dry season, rangelands have low energy content, and hence, lower glucose concentration maybe ascribed to lower dietary intake of energy [19]. Blood metabolites such as glucose and total protein could be affected by different factors such as diet, chemical composition of plant species, rumen fermentation, plant metabolites, water consumption, and passage rates. There is, therefore, a need to measure these aforementioned factors to accurately understand blood biochemistry of Zulu sheep. Blood urea concentration can be inversely related to the efficiency of nitrogen utilization and its reduction is generally associated with an increase in the efficiency of nitrogen utilization [25]. Therefore, the positive correlation on body weight against globulin, total protein, creatinine, and β-hydroxyl-butyrate could probably suggest that Nguni sheep utilize amino acids more efficiently for growth and development. The finding that total protein was positively correlated with albumin and globulin concentrations could be attributed to higher dietary crude protein concentrations from the forage. This could indicate that indigenous Nguni sheep are adapted to low protein diets.

5 Conclusion

Serum biochemistry of Zulu sheep varied with rangeland type, season, and their interactive effect. A decline in body weight and body condition score of Zulu sheep during dry season suggest a need of supplementary feeding during this period. The rangeland and seasonal variations of the biochemical profile suggests a need to consider these factors when keeping Zulu sheep because they can influence nutritional status, health status, and performance.