http://orcid.org/0000-0002-7398-2653
ABSTRACT
Aims: To examine a range of udder and teat traits in Romney ewes and to describe the frequency with which different scores occur, and to investigate associations between lamb survival to weaning and ewe udder and teat scores.
Methods: Mixed-age, mature Romney ewes (n = 1,009) were enrolled from a commercial sheep flock located in the Wellington region of New Zealand in January 2017. A range of udder and teat traits were scored in all ewes, using visual assessment and palpation, at pre-mating (February), pre-lambing (October), docking (November) and weaning (January 2018). During the lambing period each newborn lamb was matched to its dam, with lamb mortalities recorded until weaning. Associations between udder and teat scores and lamb survival to weaning were examined using multivariable models for each udder-scoring time.
Results: Records from 981 ewes and 1,822 live-born lambs were included in analyses, with 252 (13.8%) lambs recorded dead between birth and weaning. Lambs born to ewes with pre-mating udder scores of lump or hard had 4.9 (95% CI = 2.6–9.6, p = 0.003) and 3.0 (95% CI = 1.5–6.1, p < 0.001) increased odds of failure to survive to weaning, respectively, compared with lambs whose dams had normal udder scores. Lambs born to ewes with mastitis at docking or weaning had 3.0 (95% CI = 1.5–5.9, p = 0.001) and 3.9 (95% CI = 1.3–11.6, p = 0.013) increased odds of failure to survive to weaning, respectively, compared with lambs whose dams did not have mastitis. Offspring of dams with asymmetrical udders at docking or weaning had 3.3 (95% CI = 2.2–4.9, p < 0.001) and 2.5 (95% CI = 1.5–4.0, p < 0.001) increased odds of failure to survive, respectively, compared with lambs whose dams had symmetrical udders.
Conclusion and Clinical Relevance: Pre-mating udder palpation scores of hard or lump were associated with increased odds of lambs not surviving to weaning compared with normal scores, and could be used to identify ewes that are likely to be unsuitable for retaining in the breeding flock. Farmers could also use clinical mastitis scores and udder symmetry scores at docking or weaning to identify ewes whose lambs had greater odds of failure to survive to weaning. However these scores do not provide an indication of future performance, therefore further investigation into the impact of the present season’s score on future seasons’ lamb survival is required.
Introduction
The majority of income for New Zealand commercial sheep flocks is through the sale of lambs. Therefore farmers currently aim to maximise the total weight of lamb available for sale, which is a combination of both the number and the weight of the individual lambs. Lambs are solely dependent on their dams for milk for survival in early life, with milk remaining an important source of digestible energy and protein to weaning late in lactation (Hayman et al. Citation1955; Clark Citation1980). It is well established that perinatal and neonatal lamb loss is a significant issue for sheep farmers (Stafford Citation2013; Dwyer et al. Citation2016; Allworth et al. Citation2017), and that ewes with defective udders contribute to this loss (Hayman et al. Citation1955; Watson and Buswell Citation1984). However, there appears to have been little recent scientific investigation of udder morphology in New Zealand.
Data from commercial New Zealand flocks suggests that between 2–6% of ewes have defective udders at weaning (Clark Citation1980; Peterson et al. Citation2017; West et al. Citation2017). Internationally, udder defects are recognised as important causes of wastage of ewes, as a result of increased on-farm mortality and increased premature culling (Madel Citation1981; Watson and Buswell Citation1984; Annett et al. Citation2011). In New Zealand, a recent survey indicated that >85% of commercial farmers examined their ewes’ udders at least once yearly (Corner-Thomas et al. Citation2016). However, in that survey, the timing of the examination and subsequent fate of ewes were not determined, although presumably the udder examination was used to assist in culling decisions.
There is currently no standardised udder scoring method that New Zealand sheep farmers can use, and the optimal time to identify ewes that are unlikely to successfully rear their lambs is unknown. Therefore ewes may be culled unnecessarily or, conversely, ewes that are not suitable for lamb rearing may be retained within the flock. Udder morphology scoring is commonly performed in dairy ewes to improve both machine milkability and ewe udder health (Casu et al. Citation2006, Citation2010). However, there appears to be little data regarding application and relevance of udder morphology scores in non-dairy breeds.
The aims of the present study were to firstly, examine a range of udder and teat traits in Romney ewes and to describe the frequency with which different scores occur at four key management times; pre-mating, pre-lambing, docking and weaning, and secondly, to investigate associations between lamb survival to weaning and dam udder and teat scores. It was hypothesised that lambs born to ewes with poor udder and teat scores would have lower survival than those born to ewes with more desirable udder and teat scores.
Materials and methods
Farm and animals
The study utilised data collected during 2017 from mixed-age, mature Romney ewes that were born in 2013 or 2014 and were part of a commercial sheep flock located near Masterton, in the Wellington region of New Zealand. Ewes were individually identified using both an electronic identification tag and a visual identification tag (Allflex, Palmerston North, NZ). All ewes enrolled in the study flock had lambed previously. All ewes and their lambs were grazed under commercial grazing conditions on pasture containing predominantly perennial ryegrass (Lolium perenne) and white clover (Trifolium repens).
All procedures were approved by the Massey University Animal Ethics Committee.
Reproductive management and lamb survival
Ewes (n = 1,009) were joined with entire rams (n = 8) on 7 May 2017, for two oestrus cycles (34 days). Pre-mating, mean ewe liveweight was 69.3 (SD 6.3) kg. During mid-pregnancy (28 July 2017), pregnancy diagnosis was undertaken by an experienced commercial operator using transabdominal ultrasonography. Ewes were identified as either non-pregnant (no fetus), or pregnant with single (one fetus), twin (two fetuses) or triplet (three fetuses) lambs. Triplet, twin and single-bearing ewes were then split into separate groups and managed under commercial conditions so that the pasture allowance was greatest for the triplet, then twin, then single bearing ewes, although no pasture measurements were taken. Ewes were shorn in mid-pregnancy.
On 1 October 2017, 11 days prior to the planned start of lambing (pre-lambing) groups of ewes were put into individual paddocks at a rate of approximately seven, nine and 12 ewes per hectare for triplet, twin and single-bearing ewes, respectively. Prior to lambing, mean ewe liveweights were 73.6 (SD 6.4), 70.7 (SD 6.1) and 67.3 (SD 6.8) kg for triplet, twin and single-bearing ewes, respectively.
During the lambing period, intensive lambing observations were conducted twice daily. Newborn lambs (n = 1,840) were matched with their dams, identified using electronic identification tags (Allflex), and lamb sex, birth-rank (single, twin or triplet) and birth-weight were recorded. Throughout the lambing and lactation period, all lamb deaths were recorded.
On 6 and 7 November 2017, ewes and their lambs were gathered into handling facilities for weighing, ear marking, tail removal, and castration of male lambs (docking). Lambs were also weighed at weaning, which occurred on 3 January 2018. Lamb survival to weaning was defined as a lamb that was present at weaning.
Ewe udder scores
The udders and teats of all ewes were scored prior to the start of mating (17 February 2017; pre-mating), 11 days before lambing (pre-lambing), and at docking and weaning. The udder scoring system used was developed following consultation with experts from within New Zealand (veterinarians, farmers and animal scientists), and with reference to a review of existing sheep udder morphology scoring systems, as described by Casu et al. (Citation2006, Citation2010). As there were limited existing data related to non-dairy breed ewes, a range of appearance and palpation traits related to both the teats and udder were assessed, as described in . Due to the small number of ewes in some categories, some scores were subsequently combined for analyses, as described in .
Table 1. Description of the traits and scores used to assess udder morphology in ewes at different times between mating and weaning. Due to small numbers of ewes in some categories, scores were subsequently combined for analyses.
Statistical analyses
Records from 981 ewes and 1,822 lambs were included in the statistical analyses. Non-pregnant ewes (n = 16) were removed from the study flock after pregnancy diagnosis and were thus excluded from the study. A further 12 ewes were excluded due to either on-farm mortality or culling for welfare reasons. Lambs that were recorded as born-dead (n = 18) were excluded from analyses.
All statistical analyses were conducted using SAS version 9.4 (SAS Institute Inc., Cary, NC, USA). The main predictor variables for modelling were udder and teat scores, which were measured at the ewe-level. The outcome variable was lamb survival to weaning (yes or no), which was measured at the lamb-level and was also the unit of analysis. Results from each scoring time were analysed separately, with pre-mating and pre-lambing scores considered as predictive, and docking and weaning scores considered as explanatory of lamb survival to weaning. Firstly, generalised estimating equation models were used to examine the association between each predictor variable and the outcome variable. If variables were associated (p < 0.2) they were included in initial multivariable models.
Multivariable generalised estimating equation models, using an exchangeable correlation structure to account for clustering between lambs born to the same ewe, were developed for each time when udder and teat scores were recorded. Forward manual variable selection was used to build the preliminary models, with variables retained where Wald test p-values were < 0.05, after which the effect of adding variables in different orders was investigated (but without effect on the chosen model). In addition to the predictor variables determined by univariate analyses, all final models included the variables lamb sex (male or female), lamb birth rank (single, twin or triplet born) and lamb birthweight. Finally, interaction terms that were biologically plausible were considered, but no interactions were retained in final models. The fit of the final model was evaluated using the Hosmer and Lemeshow goodness of fit test (Hosmer and Lemeshow Citation2000). Probability of mortality and OR for failure of a lamb to survive to weaning, with 95% CI, for lambs born to ewes with different scores were calculated from final models.
Results
Of the 1,822 lambs, triplet, twin and single-born lambs accounted for 255 (14.0%), 1368 (75.1%) and 199 (10.9%) lambs, respectively, and 891 (48.9%) were male. The mean birthweights of triplet, twin and single-born lambs were 4.1 (SD 0.8), 5.1 (SD 0.8) and 6.1 (SD 0.9) kg, respectively. In total, 252/1822 lambs were reported as dead prior to weaning; an overall mortality rate of 13.8% from birth to weaning. Of the 252 lambs reported dead, 247 died before docking. At weaning, mean lamb age was 84.4 (SD 5.4) days, and mean weaning weights of triplet, twin and single-born lambs were 22.9 (SD 5.3), 26.7 (SD 4.5) and 32.7 (SD 5.0) kg, respectively.
Associations between lamb survival to weaning and ewe udder and teat scores
Univariate analyses
The number of ewes recorded with different scores for udder traits at each recording time is shown in , and the number of lambs born to ewes with different scores is shown in . Results of univariate analyses examining associations between different traits and survival of lambs to weaning are presented in .
Table 2. Number (%) of ewes (n = 981) in one flock that were recorded with different scores for udder traits (see ) on four occasions between mating and weaning.
Table 3. Number of lambs born to ewes in one flock that were recorded with different scores for udder traits (see ) on four occasions between mating and weaning. The number and percentage of lambs in each score category that did not survive to weaning are presented in brackets.
Table 4. Results of univariate analyses showing the OR (95% CI) for failure of a lamb to survive to weaning for lambs born to ewes in one flock that were recorded with different scores for udder traits (see ) on four occasions between mating and weaning.
At pre-mating, 6.0% of the ewes had hard udders or lumps detected by palpation, and 6.9% had one or both abnormal teats detected by palpation (). The odds of a lamb not surviving to weaning were greater if they were the offspring of ewes with udder palpation scores of hard or lump, or had one or both teats recorded as abnormal on palpation, compared to those whose dams had normal scores ().
At pre-lambing, 5.0% of the ewes had abnormal udders detected by palpation, and 6.4% of ewes had abnormal teat palpation scores (). The odds of a lamb not surviving to weaning were greater if they were the offspring of ewes with an udder palpation score of lump, or had one or both teats recorded as abnormal, compared to those whose dams had normal scores ().
At docking, the prevalence of ewes recorded with abnormal udders was 7.5%, abnormal teats was 34.9%, and clinical mastitis was 4.6% (). The odds of a lamb not surviving to weaning were greater if they were the offspring of ewes with udder palpation scores of hard or lump, or ewes with clinical mastitis, compared to those whose dams had normal udder palpation scores or did not have clinical mastitis (). However, the odds of survival to weaning was similar for offspring of dams with normal or abnormal teat palpation scores. The odds of a lamb not surviving to weaning were markedly reduced in offspring born to ewes with an udder depth score of 2, 3 or 4 compared with 5 at docking, however only 9/981 (0.9%) ewes had a score of 5 at docking.
At the weaning the prevalence of ewes with abnormal udders was 7.4%, clinical mastitis was 3.1%, and asymmetrical udders was 10.2% (). The odds of a lamb not surviving to weaning were greater if they were the offspring of ewes with udder palpation scores of hard or lump, ewes with clinical mastitis, or ewes with asymmetrical udders, compared to those whose dams had normal udder palpation scores, did not have clinical mastitis, or had symmetrical udders, respectively ().
Multivariable analyses
Pre-mating udder palpation scores were predictive of failure of lambs to survive to weaning, with the offspring of dams with udder scores of lump or hard having increased odds of failure to survive to weaning compared with lambs whose dams had normal udders ().
Table 5. Results of final multivariable modelsa showing the OR (95% CI) for failure of a lamb to survive to weaning in lambs born to ewes with different scores for udder traits (see ) recorded on four occasions between mating and weaning, with the absolute probability of mortality for lambs born to ewes with different scores.
Pre-lambing, udder palpation scores, teat palpation scores and udder symmetry scores were predictive of failure of lambs to survive to weaning (). Lambs born to ewes with udder scores of lump, or one or both teats recorded as abnormal, had increased odds of failure to survive compared with lambs whose dams had normal udders. In addition, lambs born to ewes with asymmetrical udders pre-lambing had increased odds of failure to survive compared to offspring of ewes with symmetrical udders.
At docking, udder depth, clinical mastitis and udder symmetry scores were explanatory of failure of lambs to survive to weaning (). The offspring of dams with udder depth scores of 5 or 4, compared with 2, had increased odds of failure to survive. Lambs born to ewes that had mastitis or asymmetrical udders at docking had increased odds of failure to survive, compared with lambs whose dams did not have mastitis, or had symmetrical udders, respectively.
At weaning, udder depth, clinical mastitis and udder symmetry scores were explanatory of failure of lambs to survive to weaning (). The offspring of dams with udder depth scores of 5 compared with 2, had increased odds of failure to survive. Lambs born to ewes that had mastitis or asymmetrical udders at weaning had increased odds of failure to survive, compared with lambs whose dams did not have mastitis, or had symmetrical udders, respectively.
Discussion
To the authors’ knowledge, this study is the first undertaken for many years in New Zealand that describes the prevalence of a range of udder and teat traits in Romney ewes in a commercial flock. Comparable data tend to focus on one specific trait, e.g. mastitis, rather than considering a range of traits (Quinlivan Citation1968), or udders may only have been classified simply as defective or normal (Hayman et al. Citation1955; Quinlivan Citation1968). The results of the multivariable analyses in the present study support the hypothesis that lambs born to ewes with poor udder and teat scores would have lower survival than lambs born to ewes with more desirable udder and teat scores. However, these relationships varied between traits and between observation times.
Physical palpation allows detection of abnormalities in the udders of ewes. The percentage of ewes with normal udder palpation scores varied between 92.6–95.0%, with the remainder having palpation scores classified as either lump or hard. This result is consistent with previous studies, in which between 2.3–6.0% of ewes were reported to have defective udders (Hayman et al. Citation1955; Quinlivan Citation1968) however in those studies the type of defect was not well defined. The findings from the present study support the practice of hands-on udder palpation prior to breeding.
For commercial farmers, it would likely be optimal if they could identify ewes that are unsuitable for retention in the breeding flock prior to breeding, and if they were able to make culling decisions based on udder health at only one time during the year. Early identification of these unsuitable ewes could reduce unnecessary feed and management inputs, as these resources would be more efficiently utilised by those ewes that are more likely to successfully rear their offspring to weaning. In this study, pre-mating udder palpation score was associated with lamb survival, with odds of failure to survive to weaning being greater for lambs born to ewes with scores of lump or hard compared with normal. This finding indicates farmers should consider proactively identifying these ewes prior to breeding.
A number of traits measured prior to lambing, udder palpation, teat palpation and udder symmetry, were predictive of lamb survival to weaning. Although abnormal udder and teat scores were associated with increased lamb mortality in the current season, further work is required to assess repeatability of scores in the subsequent season, or whether these abnormalities would be suitable for treatment.
The docking and weaning models were retrospective, in that the majority of lamb deaths occurred prior to docking, so at these times it is likely that ewes had already lost either all or some of their lambs. The odds of failure to survive to weaning was greater for lambs whose dams had mastitis at docking and weaning compared with dams who did not have mastitis, in agreement with previous reports (Hayman et al. Citation1955; Arsenault et al. Citation2008). The percentage of ewes with mastitis in the present study varied between 0.8–4.6%, similar to the findings of Quinlivan (Citation1968, 1972) and Clark (Citation1972), and slightly less than that reported by Peterson et al. (Citation2017). Presence of clinical mastitis is something farmers can readily assess when ewes are yarded for other management interventions during lactation, for example at docking. In a review of mastitis in dairy small ruminants, Bergonier et al. (Citation2003) discussed the chronic persistence of small ruminant mastitis, with elimination relying on culling of affected animals or targeted treatment. However, at present, it is not known if non-dairy breed ewes that have mastitis in one season are more likely to have mastitis in a subsequent season than ewes without mastitis, or if the mastitis will be associated with an increased risk of undesirable udder scores at the following breeding. Further investigations to answer this question in longitudinal studies of New Zealand commercial flocks would be of benefit.
In the present study, udder symmetry at docking and weaning were associated with lamb survival, with the odds of failing to survive to weaning being greater in lambs whose dams had asymmetrical compared with symmetrical udders. To the author’s knowledge, there is no previous description of the relationship between udder symmetry and lamb survival and it is a quick and easy trait for farmers to assess. Udder symmetry could be used to identify ewes that have likely lost a lamb in the current lactation, however, it is unknown if asymmetry in one lactation will affect subsequent lactation performance and lamb survival in the following year. Further longitudinal studies in New Zealand commercial flocks are required to assess this.
Udder morphology scores described in milking-sheep, such as udder suspension, udder separation and teat placement, appeared to have little association with lamb survival to weaning. The only morphology score that was associated with failure to survive to weaning in the multivariable models was udder depth, at both docking and weaning. The inclusion of udder depth during lactation is not surprising, as an udder depth score of five was likely identifying ewes that were not lactating. Combined, the present data suggest the use of morphological scores developed for dairy sheep are of limited value in non-dairy breeds, in the context of predicting lamb survival to weaning.
In the present study, small numbers of ewes in some categories, e.g. udder palpation scores 3–6, meant scores had to be combined for analysis. However, the merged scores would be easy and quick for farmers to utilise on-farm, e.g. udder palpation scores of normal vs. lump vs. hard. Another limitation of the study was that it was performed on only one commercial farm over one year. However, the farm used is representative of a North Island hill country commercial sheep farm, based on flock and farm size and productivity parameters (Anonymous Citation2018). The lamb mortality rate of 14.7% also reflects the typically reported lamb mortality of 15% (Stafford Citation2013). In addition, the prevalence of the various udder and teat abnormalities were comparable to those previously reported (Hayman et al. Citation1955; Quinlivan Citation1968, 1972; Clark Citation1972). It is likely the results and conclusions drawn from the present study can be extrapolated to the wider New Zealand commercial sheep population, but further longitudinal studies on more flocks and farms are required to both validate these results and to provide more robust support for any recommendations.
In conclusion, pre-mating udder palpation scores of hard or lump were associated with increased odds of lambs not surviving to weaning compared with normal scores, and could be used to identify ewes that are likely to be unsuitable for retaining in the breeding flock. Farmers could also use the udder symmetry scores, clinical mastitis scores and udder depth scores at docking or weaning to identify ewes whose lambs had greater odds of failure to survive to weaning. However these scores do not provide an indication of future performance, therefore further investigation into the impact of the present season’s score on future seasons’ lamb survival is required. These results should also be considered in association with the results of our companion paper examining relationships between udder traits and lamb growth rates to weaning (Griffiths et al. Citation2019).
Acknowledgements
The authors would like to thank the farm manager, shepherd and technical staff at Massey University (particularly Geoff Purchas and Dean Burnham) for their invaluable assistance during the study. In addition, the help of staff and students at Taratahi Agricultural Training Centre was greatly appreciated. This research was funded by Beef + Lamb New Zealand and the C. Alma Baker Trust.
ORCID
R. A. Corner-Thomas http://orcid.org/0000-0002-7398-2653
P. R. Kenyon http://orcid.org/0000-0003-1131-0736
References
- Allworth MB, Wrigley HA, Cowling A. Fetal and lamb losses from pregnancy scanning to lamb marking in commercial sheep flocks in southern New South Wales. Animal Production Science 57, 2060–65, 2017 doi: 10.1071/AN16166
- Annett RW, Carson AF, Dawson LER, Irwin D, Gordon AW, Kilpatrick DJ. Comparison of the longevity and lifetime performance of Scottish Blackface ewes and their crosses within hill sheep flocks. Animal 5, 347–55, 2011 doi: 10.1017/S1751731110002107
- *Anonymous. Sheep and Beef Farm Survey Analysis https://beeflambnz.com/data-tools/benchmark-your-farm (accessed 7 March 2019). Beef + Lamb New Zealand, Wellington, NZ, 2018
- Arsenault J, Dubreuil P, Higgins R, Belanger D. Risk factors and impacts of clinical and subclinical mastitis in commercial meat-producing sheep flocks in Quebec, Canada. Preventative Veterinary Medicine 87, 373–93, 2008 doi: 10.1016/j.prevetmed.2008.05.006
- Bergonier D, de Crémouxb R, Ruppc R, Lagriffould G, Berthelota X. Mastitis of dairy small ruminants. Veterinary Research 34, 698–716, 2003 doi: 10.1051/vetres:2003030
- Casu S, Pernazza I, Carta A. Feasibility of a linear scoring method of udder morphology for the selection scheme of Sardinian sheep. Journal of Dairy Science 89, 2200–09, 2006 doi: 10.3168/jds.S0022-0302(06)72290-1
- Casu S, Sechi S, Salaris SL, Carta A. Phenotypic and genetic relationships between udder morphology and udder health in dairy ewes. Small Ruminant Research 88, 77–83, 2010 doi: 10.1016/j.smallrumres.2009.12.013
- *Clark RG. Field observations on ovine mastitis. Proceedings of the 2nd Annual Seminar of the Society of Sheep and Beef Cattle Veterinarians of the New Zealand Veterinary Association. Pp 47–54, 1972
- *Clark RG. Ovine Mammary Disease – A Review. Proceedings of the 10th Annual Seminar of the Society of Sheep and Beef Cattle Veterinarians of the New Zealand Veterinary Association. Pp 16–29, 1980
- Corner-Thomas RA, Kenyon PR, Morris ST, Ridler AL, Hickson RE, Greer AW, Logan CM, Blair HT. The use of farm-management tools by New Zealand sheep farmers: changes with time. Proceedings of the New Zealand Society of Animal Production Volume 76, 78–80, 2016
- Dwyer CM, Conington J, Corbiere F, Holmoy IH, Muri K, Nowak R, Rooke J, Vipond J, Gautier JM. Improving neonatal survival in small ruminants: science into practice. Animal 10, 449–59, 2016 doi: 10.1017/S1751731115001974
- Griffiths KJ, Ridler AL, Compton CWR, Corner-Thomas RA, Kenyon PR. Associations between lamb growth to weaning and dam udder and teat scores. New Zealand Veterinary Journal 67, 172–9, 2019
- Hayman RH, Turner HN, Turton E. Observations on survival and growth to weaning of lambs from ewes with defective udders. Australian Journal of Agricultural Research 6, 446–55, 1955 doi: 10.1071/AR9550446
- *Hosmer D, Lemeshow S. Applied Logistic Regression. 2nd Edtn. J. Wiley & Sons Inc., Hoboken, NJ, USA. 2000
- Madel AJ. Observations on the mammary glands of culled ewes at the time of slaughter. Veterinary Record 109, 362–63, 1981 doi: 10.1136/vr.109.16.362
- Peterson SW, Nieper B, Collett, MG, Grinberg A. An investigation of mastitis in a hill-country sheep flock. Proceedings of the New Zealand Society of Animal Production Volume 77, 114–16, 2017
- Quinlivan TD. Survey observations on ovine mastitis in New Zealand stud Romney flocks. New Zealand Veterinary Journal 16, 149–53, 1968 doi: 10.1080/00480169.1968.33765
- Quinlivan TD. Ovine Mastitis. Proceedings 2nd Annual Seminar, Society of Sheep and Beef Cattle Veterinarians of the New Zealand Veterinary Association, Pp 32–40, 1972
- *Stafford KJ. Animal Welfare in New Zealand. New Zealand Society of Animal Production (Inc). Cambridge, New Zealand. 2013
- Watson DJ and Buswell JF. Modern aspects of sheep mastitis. British Veterinary Journal 140, 529–34, 1984 doi: 10.1016/0007-1935(84)90003-4
- *West DM, Bruere AN, Ridler AL. The Sheep: Health, Disease and Production. 4th Edtn. Massey University Press. Auckland, New Zealand. 2017
- *Non-peer-reviewed