Assessing the age of puberty of Djallonke gimmers born in rainy or dry season using progesterone measurements

S Salifu, S A Osei¹, B A Hagan, E Allegye-Cudjoe² and F K Avornyo

CSIR-Animal Research Institute P O Box 52, Nyankpala, Ghana.
ssalifuari@gmail.com
¹ Kwame Nkrumah University of Science and Technology, Department of Animal Science, Kumasi, Ghana.
² Pong-Tamale Central Veterinary Laboratory, Pong Tamale, Ghana.

Abstract

A study was carried out to determine the age of puberty of 20 Djallonke gimmers born under the two major seasons in the northern Guinea Savannah Zone of Ghana, the rainy season (n=10) and the dry season (n=10). Peripheral blood progesterone (P4) measurements were used to establish the age at which gimmers first showed ovarian activity. The age at first oestrus, age at first lambing, lambing intervals, placenta weights and lamb birth weights were also assessed. The effect of season on these reproductive parameters was determined. The Djallonke gimmers started to show ovarian activity (rise of P4) at the age of 221± 9 days, at 55.6% of adult weight, with rainy season lambed gimmers (RSLG) showing ovarian activity significantly earlier (202 ± 11 v 239 ±13 days) compared to the dry season lambed gimmers (DSLG) (P<0.05). The RSLG also went on to lamb earlier than DSLG (425± 11 v 496± 31 days) (P<0.05) and produced heavier lambs as well (1.77 ± 0.08 v 1.40± 0.13 kg). It is suggested that timing lambing to occur in the rainy season may provide a better nutritional environment for lactating ewes to nourish their lambs and for gimmers to grow faster and attain puberty earlier.

Keywords: female, Ghana, lamb, reproductive performance, West African Dwarf Sheep

Introduction

Sheep are an important livestock resource for resource-poor farmers in Northern Ghana, with farming households in this area keeping an average of 10 small ruminants (Avornyo et al, 2007). Small ruminants in general are kept primarily as a source of ready income (Amankwah et al 2012), for meat, and for cultural purposes such as contracting marriages and performing sacrifices for religious purposes among resource-poor farmers (Abassa 1995; Devendra 1994). Small ruminant production is therefore widely seen as means of reducing poverty among the rural poor in developing countries and any improvement in productivity is likely to enhance the income of households (Owen et al 2005).

Reproductive performance is a key measure of productivity among livestock (Gbangboche et al 2006). Age of puberty, age at first lambing, postpartum intervals and lambing intervals are some of most important indices of reproductive performance because of their influence on the lifetime productivity of the female sheep (Abassa 1995). These indices of reproductive performance are however subject to the influence of environmental factors, key among which is the nutritional environment (availability of feed), and it is important to understand how this influences the performance of small ruminants to facilitate planning (Gbangboche et al 2006). The vegetation of the Guinea Savannah areas of Ghana varies widely throughout the year mirroring the rainfall pattern; the quality and quantity of feed resources available for small ruminants therefore reflects this trend (Oppong-Anane 2013). The flux in feed, and hence nutrient availability, may therefore influence the reproductive performance of small ruminants, thereby affecting productivity (Almeida et al 2006; Cardoso and Alameida 2013). Management decisions regarding the optimum season of the year to breed sheep will be greatly helped by data showing the best season to time lambing.

This is especially true for a tropical breed like the Djallonke which does not undergo seasonal anoestrus (Jainudeen et al 2000) and exhibits oestrus cycles throughout the year if environmental conditions such as feed availability permit.

Measuring levels of reproductive hormones such as progesterone is an important tool for elucidating the inner workings of the reproductive system in animals, and this has been used in previous studies to monitor reproductive events such as onset of puberty and postpartum return to oestrus in sheep and goats (Khanum et al 2006; Valasi et al 2013).

This study was therefore undertaken to assess the age of puberty and reproductive performance of Djallonke gimmers and to estimate the influence of season of lambing on the onset of puberty on lambs born inthe rainy season or the dry season of the Guinea Savannah Zone of Ghana.

Materials and methods

Study area

The study was carried out at the Pong Tamale Livestock Breeding Station and the Pong Tamale Central Veterinary Laboratory in Savelugu/Nanton district of Ghana, located on Longitude 0⁰ 49” N and Latitude 9 ⁰ 40” W, about 32 km from the Northern Region capital of Tamale. The area falls within the Guinea Savannah vegetative zone of Ghana and experiences a unimodal rainfall pattern throughout the year with mean annual rainfall of 1 043 mm. There are two distinct seasons, a rainy season covering the months of May to September, and a dry season which begins in October and ends in late May. Peak rainfall for the rainy season is confined to the months of August and September. Rainfall for the peak period represents 40% of rain for the entire rainy season.

Experimental animals and management

Twenty Djallonke gimmers were monitored from the time of weaning, until they displayed first oestrus. Ten of the selected gimmers were born in the rainy-season in June and July while the other ten were born in the dry season, in November and December.

The experimental animals were grazed on pastures of Stylosanthes hamata, Panicum minimum and Cajanus cajan fodder from 9 am to 5 pm daily in the rainy period, but in the dry season, when the vegetation had dried up, the animals were fed crop residues from some locally cultivated crops such as Cajanus cajan waste, groundnut tops and cassava peels. Water was offered to the animals ad libitum.

Routine deworming against helminths was done every month in the rainy season and every other month in the dry season using Albendazole dewormer 2.5% (manufactured by Kela N.V., Belgium). The animals were also vaccinated against the peste des petits ruminants (PPR) once a year using PPR-VAC (manufactured in Botswana).

Progesterone monitoring

Blood samples were taken from the animals every other day by jugular venipuncture and the samples were stored on ice until they were centrifuged later at the laboratory and the serum harvested and stored at -40 ^oC, pending analysis for progesterone. A Solid Phase Enzyme Linked immunosorbent assay (ELISA) kit supplied by DRG International New Jersey, USA was used to test the samples for progesterone. The assay was performed in duplicate. Inter and intra assay coefficient of variation were 7.04% and 3.81% respectively. Assay sensitivity was 0.045 ng/ml. The ELISA test plates were read with a BioTek^® Instruments ELISA plate reader (ELx800 model) through a 450 nm filter. The absorbance/optical density (OD) values obtained from the reader were used to compute the concentration of progesterone in the samples. This was done by plotting a standard curve for each assay using 7 standards (in duplicate) with known concentrations. The concentrations of the samples collected were then interpolated from the standard curve using the OD values generated.

All samples that showed progesterone concentration above a threshold of 1 ng/ml for two consecutive tests was taken to indicate the presence of a corpus luteum (Mukasa-Mugerwa and Ezaz 1991; Pineda and Dooley 2008).

Monitoring of oestrus

Two intact rams were fitted with harnesses (raddle) fitted with a crayon and allowed to run with the females. The rams which mated with the females left streaks of crayon marks on the rumps of the females. This was taken to mean the display of oestrus by the female, occasioning the mating. To test for pregnancy, serum samples of mated gimmers were tested the 21 ^st day and the 45^th day after mating. Animals that continued to show elevated levels of progesterone were assumed to be pregnant.

Data collected and statistical analysis

Data was collected from the gimmers on age at first progesterone rise, age at first overt oestrus, age at first parturition/lambing, lamb birth weights, placenta weight and gestation length. Monthly weights of all animals was taken and growth rates were computed from these. The animals were also scored for body condition using the standard of Russel (1984) where 0= extremely emaciated, 1= spinous process prominent and sharp, 2= spinous process prominent but smooth, 3= spinous processes felt only as smooth round elevations, 4= spinous process felt only with pressure, 5= extreme fatness).

The GLM procedure of SAS (SAS Institute Inc 2014) was used to analyse the weight and reproductive parameters of the gimmers using season of birth as a fixed effect. The sex of lamb was included in the model for analysis of birth weight, placenta weight and gestation length.

Results

Effect of season on weight dynamics of pubertal gimmers

The Table 1 shows growth performance of Djallonke gimmers in the study under the two seasons. The rainy season lambed gimmers (RSLG) grew at a faster rate (P=0.04) and had a better body condition score (BCS) (P=0.001) compared to the dry season lambed gimmers.

Effect of season of birth on first ovarian activity

The mean age at which gimmers first showed ovarian activity (evidenced by the first progesterone rise above the 1 ng/ml threshold) was 221±9 days with a range of 160 to 310 days. The RSLG however experienced first progesterone rise 36 days earlier than the DSLG (P=0.045) (Table 2). The first display of oestrus, which was preceded by the first rise of progesterone, however occurred at a mean age of 289±15 days, about 69 days after the first progesterone rise. There was no seasonal difference in age at first oestrus display (P=0.079). Mean weight at first progesterone rise and mean weight at first mating were 12.1 kg and 16.0 kg respectively. The mean weight at first progesterone rise and mean weight at mating between seasons were not statistically different (P=0.468 and P=0.438 respectively) (Table 2). The rainy season lambed gimmers went on to lamb 71 days earlier than the dry season lambed gimmers (P=0.042) and also produced heavier lambs (P=0.032). Gestation length, placenta weight and pregnancy anabolism for the gimmers did not differ significantly between seasons (P>0.05).

Progesterone profiles of pubertal gimmers

Progesterone concentration was at basal levels (mean= 0.160±0.005 ng/ml) in blood samples taken from all the gimmers at the beginning of the trial and only increased beyond the 1 ng/ml threshold when the gimmers reached a mean age of 221±9 days. Gimmers showed brief elevations in serum progesterone concentration (mean=1.21ng/ml) before the first display of oestrus. The first progesterone elevations were of short duration (lasting 2 to 4 days, with a mean of 2.2 days) and were not accompanied by any overt oestrus. There was no statistically significant difference between seasons for concentration of progesterone at first rise (1.25 ng/ml and 1.15 ng/ml for the rainy and dry seasons respectively) (P=0.249). The period from the first progesterone rise to the first overt oestrus display (as indicated by display of oestrus and mating) varied among individual gimmers and showed an average of 1.4 rises in progesterone above basal levels in the intervening period (Figure 1). Figures 1 and 2 show some typical patterns exhibited by gimmers coming into puberty for the RSLG and DSLG respectively. Some gimmers (CD 1, Figure 1) displayed a prolonged luteal phase following mating.

Figure 1. Progesterone profile of a rainy season lambed gimmer showing initial elevations of progesterone before oestrus. Gimmer CD1 displayed progesterone peaks lasting 2 days and 12 days before displaying oestrus and being mated. A third luteal phase lasting 25 days may have been an early embryonic death. Gimmer CD5 displayed 3 progesterone elevations lasting 2, 10 and 12 days before displaying oestrus. Black arrows represent mating.

Figure 2. Progesterone profiles of two dry season lambed Djallonke gimmers. Black vertical arrows indicate mating.

Discussion

In spite of the small number of animals tested (10 in the wet season and 10 in the dry season), the mean growth rate of the gimmers in this study were consistent with growth rates in the range of 25-49 g/day reported by Bosso et al (2007) and Gbangboche et al (2006) for Djallonké females aged 120 days and older. The superior growth rate of the rainy season-lambed gimmers may be attributed to better nourishment they received from their mothers, who had access to a relatively good supply of pasture while they lactated. Tibbo (2006), working with Menz lambs also observed higher growth rates of lambs in the rainy season compared to the dry season (74 vs 54 g per day) and cited pasture availability in the rainy season as the reason for superior growth rate in that season. Other studies (Abegaz et al 2000; Mukasa-Mugerwa et al 1994) confirm our findings.

Body weight is reported to be a better predictor of age at puberty than chronological age. Ibrahim (1998) reported that puberty usually occurs when a threshold body weight has been attained by the animal. Faster growing animals therefore attain puberty earlier than slower growing ones (Foster and Nagatani 1999; McDonald et al 2010; Pineda and Dooley 2008; Senger 2005). Overall, the RSLG grew at a faster rate than the DSLG (45.3g/d vs. 37.1 g/d, Table 1) and they therefore reached the threshold body weight at which ovarian activity was initiated earlier than the dry season gimmers as a result of the observed difference in growth rate. In spite of the significant difference in age at first progesterone rise, however, the gimmers reached puberty at a similar weight for both groups (13.1 kg vs. 12.7 kg) (P>0.05). This observation was previously reported by Dyrmundsson (1981) and Foster and Nagatani (1999), who associated fast body growth with the early onset of puberty. Noakes et al (2001) have also reported that weight is more influential than chronologic age in determining the time of puberty. The weight at first progesterone rise in this study closely matches the results obtained by Obese (1994) working with Djallonké gimmers in the humid southern zone of Ghana. In that study, puberty was attained when the gimmers reached 55.6% of their mature body weight. The rainy season and dry season born gimmers in this study, respectively attained puberty at 56.5% and 54.7% of their mature body weight (23.5 kg). Ibrahim (1998) reported that gimmers would usually attain puberty when they have attained 45 - 60% of their adult body weight.

The patterns of serum progesterone concentration observed for gimmers approaching puberty in this study were consistent with those observed by Sutama et al (1988) among adolescent Javanese thin-tailed sheep. Their study revealed that 83% of ewe lambs showed one or more significant elevations in peripheral progesterone level before their first ovulation. Such transient increases in progesterone in pubertal ewes before the first oestrus have also been previously observed (Berardinelli et al 1980; Foster and Ryan, 1979; Keisler et al 1983). The pronounced progesterone peaks that preceded ovulation were thought to have originated from luteinized follicles that failed to ovulate, as has been documented by Bartlewski et al (1999). It has been reported (Brown et al 2014; Senger 2005) that priming of the central nervous system with progesterone is required before the full display of oestrus is possible.

Conclusion

• It is concluded that Djallonke gimmers that were born in the rainy season reached puberty earlier than those that were lambed in the dry season.
  
  
• Gimmers that were born in the rainy season also went on to lamb earlier than their dry season born counterparts.
  
  
• The earlier onset of puberty among gimmers born in the rainy season was attributed to the comparatively better nourishment they received from their mothers who has access to abundant grazing in the rainy season.
  
  
• It is therefore probable that improving the quality and quantity of feed for gimmers may speed up the onset of puberty, age at first lambing and improve life time reproductive performance.
  
  
• Most reproductive indices were favourable for gimmers lambed in the rainy season.

Acknowledgements

The authors would like to thank the Pong Tamale Livestock Breeding Station and Pong Tamale Central Laboratory which provided the animals and laboratory space and the personnel who helped in conducting this experiment.

References

Abassa K P 1995 Reproductive losses in small ruminants in Sub-Saharan Africa : A review. ILCA working document,Addis Abba, Ethiopia. Retrieved from https://cgspace.cgiar.org/bitstream/handle/10568/4229/ILCA_WD.pdf?sequence=2&isAllowed=y

Abegaz S, Gemeda D, Rege J E O, Van Wyk J B, Neser F W C and Erasmus G J 2000 Early growth, survival and litter size in Ethiopian Horro sheep. South African Journal of Animal Science, 30(4). https://doi.org/10.4314/sajas.v30i4.3884

Almeida A M, Schwalbach L M, Waal H O De, Greyling J P C and Cardoso L A 2006 The effect of supplementation on productive performance of Boer goat bucks fed winter veld hay. Tropical Animal Health and Production, 38(5), 443–449.

Amankwah K, Klerkx L, Oosting S J, Sakyi-Dawson O, Van Der Zijpp A J and Millar D 2012 Diagnosing constraints to market participation of small ruminant producers in Northern Ghana: An innovation systems analysis.NJAS - Wageningen Journal of Life Sciences, 60– 63, 37–47. https://doi.org/10.1016/j.njas.2012.06.002

Avornyo F K, Otchere E O and Mbii P 2007 A baseline survey of small ruminant project communities in Northern Region. In J Bruce, N Karbo, V A Clottey, F Adongo, M Alebikiya & M Asobayire (Eds.), National conference on participatory agricultural research and development(pp. 109–117).

Bartlewski P M, Beard A P and Rawlings N C 1999 Ovarian function in ewes during the transition from breeding season to anoestrus. Animal Reproduction Science, 57(1–2), 51–66.

Berardinelli J G, Dailey R A, Butcher R L and Inskeep E K 1980 Source of circulating Progesterone in prepubertal ewes. Biology of Reproduction, 22(2), 233 - 236

Bosso, N. A., Cisse, M F, van der Waaij E H, Fall A and van Arendonk J A M 2007 Genetic and phenotypic parameters of body weight in West African Dwarf goat and Djallonke sheep, 67, 271–278.

Brown H M, Fabre Nys C, Cognié J and Scaramuzzi R J 2014 Short oestrous cycles in sheep during anoestrus involve defects in progesterone biosynthesis and luteal neovascularisation. Reproduction, 147(3), 357–367. https://doi.org/10.1530/REP-13-0400

Cardoso L A and Alameida A M 2013 Seasonal weight loss – an assessment of losses and implications for animal welfare and production in the tropics: Southern Africa and Western Australia as case studies. Enhancing animal welfare and farmer income through strategic animal feeding - Some case studies, FAO Animal health and production paper 175, pp 37-44

Devendra C 1994 Small ruminants’ potential value and contribution to sustainable development. Outlook Agric., 23, 97-103.

Dyrmundsson O R 1981 Natural factors affecting puberty and reproductive performance in ewe lambs: a review. Livestock Production Science, 8, 55–65.

Foster D L and Nagatani S 1999 Physiological perspectives on leptin as a regulator of reproduction: role in timing puberty. Biology of Reproduction, 60(2), 205–215. https://doi.org/10.1095/biolreprod60.2.205

Foster D L and Ryan K D 1979 Endocrine mechanisms governing transition into adulthood: a marked decrease in inhibitory feedback action of oestradiol on tonic secretion of luteinizing hormone in the lamb during puberty. Endocrinology, 105, 896–904.

Gbangboche A B, Youssao A K I, Senou M, Adamou-Ndiaye M, Ahissou A, Farnir F and Leroy P L 2006 Examination of non-genetic factors affecting the growth performance of djallonke sheep in soudanian zone at the Okpara breeding farm of Benin. Tropical Animal Health and Production, 38, 55–64.

Ibrahim H 1998 Small ruminant production techniques (No. 3). ILRI Training Manual 3. Nairobi.

Jainudeen M R, Wahid H and Hafez E S E 2000 Sheep and goats. In E S E Hafez & B Hafez (Eds.), Reproduction in farm animals (7th edition). Baltimore, USA: Lippincott Williams & Wilkins, pp. 172–181

Keisler D H, Inskeep E K and Dailey R A 1983 First luteal tissue in ewe lambs: influence on subsequent ovarian activity and response to hysterectomy. Journal of Animal Science,57 (1), 150-156

Khanum S A, Hussain M and Kausar R 2006 Manipulation of estrous cycle in Dwarf goat (Capra hircus) using estrumate under different management conditions. Animal Reproduction Science, 92(1–2), 97–106

McDonald P, Edwards R A, Greenhalgh J F D, Morgan C A, Sinclair L A, and Wilkinson R G 2010 Animal nutrition (7th ed.). London: Prentice Hall. pp 361 -362.

Mukasa-Mugerwa E and Ezaz Z 1991 Resumption of post-partum oestrous behaviour and associated plasma progesterone profiles in Menz ewes. Animal Production, Volume 52(2), 297–300.

Mukasa-Mugerwa E, Said A N, Lahlou-Kassi A, Sherington J and Mutiga E R 1994 Birth weight as a risk factor for perinatal lamb mortality, and the effects of stage of pregnant ewe supplementation and gestation weight gain in Ethiopian Menz sheep. Preventive Veterinary Medicine, 19 (1), pp 45-56

Noakes D E, Parkinson T J and England G C W 2001 Arthur's Veterinary Reproduction and Obstetrics. 8^th edition. Elsevier Limited, Philadelphia, USA. Pp 3-848

Oppong-Anane K 2013 Cassava as Animal Feed in Ghana: Past, Present and Future. (B Berhanu, L Cheikh, & P S Harinder Eds.), Food and Agriculture Organization of the United Nations. Accra.pp. 1-51.

Owen E, Kitalyi A, Jayasuriya N and Smith T 2005 Livestock and wealth creation: improving the husbandry of animals kept by resource-poor people in developing countries. Livestock and Wealth Creation: Improving the Husbandry of Animals Kept by Resource-Poor People in Developing Countries. pp. 500.

Pineda M and Dooley M P 2008 Veterinary endocrinology and reproduction. (M. Pineda & M. P. Dooley, Eds.), McDonald’s Veterinary endocrinology and reproduction (5th ed.). Wiley, 2008.

Russel A J F 1984 Means of assessing the adequacy of nutrition of pregnant ewes. Livestock Production Science, 11(4), 429–436. https://doi.org/10.1016/0301-6226(84)90054-X

SAS Institute Inc. 2014 SAS Institute Inc. MarketLine Company Profile. SAS Institute Inc

Senger P L 2005 Pathways to Pregnancy and Parturition. (2^nd Ed.), Current Conceptions Inc. Pp 1 - 344

Sutama I K, Edey T N and Fletcher I C 1988 Oestrous Cycle dynamics in Peri-pubertal and mature Javanese thin-tail sheep, 16, 61–70

Tibbo M 2006 Productivity and health of indigenous sheep breeds and crossbreds in the Central Ethiopian Highlands. Swedish University of Agricultural Sciences. p. 31.

Valasi I, Theodosiadou E, Fthenakis G C, Papanikolaou T, Deligiannis C, Kalogiannis D and Amiridis G S 2013 Endocrinological profile and follicular development in cyclic ewes subjected to repeated ovum pick-up. Animal Reproduction Science, 138(3–4), 180–187

Received 8 October 2018; Accepted 8 November 2018; Published 2 December 2018

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