Small Ruminant Research 184 (2020) 106009

Contents lists available at ScienceDirect

Small Ruminant Research

journal homepage: www.elsevier.com/locate/smallrumres

Ovine mammary morphology and associations with milk production, T

milkability and animal selection
Aris Pourlis*
Laboratory of Anatomy Histology and Embryology, Faculty of Veterinary Medicine, University of Thessaly, Greece

A R T I C LE I N FO A B S T R A C T

Keywords: In current dairy sheep management, there is a widespread trend to improve the morphology of the udder for
Sheep machine- and hand-milking ability. The purpose of this review is to present the literature regarding udder
Udder morphological traits related to milk production of sheep. The ovine udder consists of two mammary glands.
Teat Various techniques have been employed to appraise the mammary morphology and anatomy. Articles referring
Ultrasonography
to all these methods are referred to. The typology and the linear scoring of udders and their measurable variables
Quantitative trait loci
are described. Non-invasive methods, e.g., ultrasonography or digital image analysis, are assessed. Relationships
between morphological and production traits are analyzed. Comparative results of quantitative trait loci de-
tection for udder morphology traits in dairy sheep are included. Papers related to milkability are evaluated
within the udder and teat morphological context. Use of mammary morphological traits is recommended in
order to improve the morphology of the udder and, accordingly, the milkability of the sheep. Thus, their in-
clusion in programs of genetic improvement could increase the productivity of the animals.

1. Introduction
Milk production represents an important sector of agriculture, in
which, several ruminant species are used for the production of milk and
dairy products. Among ruminants, sheep dairy production holds an
important share. In modern sheep husbandry, overall aim is to achieve
increased productivity ensuring, at the same time, high milk quality and
better working conditions. Machine-milking is a fundamental tech-
nology to achieve these goals, and udder morphology, which affects
milking procedures, is important for optimum adaptation of ewes to the
milking environment (Dzidic et al., 2004). Within this context, several
traits have become of interest for dairy sheep genetic selection: ma-
chine-milking ability and udder morphology, resistance to diseases,
milk nutritional value, safety of milk, adaptation to local breeding
conditions, feed efficiency, reproduction traits and lamb meat produc-
tion (Carta et al., 2009). Among them, udder morphology / anatomy
plays a crucial role. The increase of the use of machine-milking resulted
in the increase of studies, which deal with the relation of the udder with
milk production. Udder morphology is a key factor, which affects the
(mainly machine-) milkability of the ewes, because the udder must fit
into the clusters (de la Fuente et al., 1996).
The perfect udder for machine milking was called ‘udder machine’
(Mikus, 1978). According to Mikus, the ‘udder machine’ must be well
attached, must have vertical teats of medium size and low cistern
height. Many publication regarding sheep husbandry have presented
many optimum values for the various udder traits. The majority of the
values is similar and applicable to the majority of the dairy breeds.
Better knowledge of the morphological variation would allow the
identification of those mammary traits most suitable for incorporation
into selection programs.
The objectives of this review were to collect and evaluate the
methods of udder appraisal and the results of the studies, which have
been carried out thusfar. In addition, genetic parameters of udder type
traits and especially their relationship with milk yield will be presented
and discussed. Modern methods to assess udder morphology and
milkability in dairy sheep will be surveyed.
2. Structure of the ovine udder
The ovine udder is in the inguinal region and comprises two in-
dependent mammary glands, one on each side of the ventral midline.
The glands are covered by fibroelastic connective tissue (apparatus
suspensorius mammarum) and separated by a clearly defined and inter-
mediate wall of connective tissue (ligamentum suspensoris uber). The
strength of this ligament normally produces the presence of an inter-
mmamary groove (sulcus intermammarius) between the glands, which

⁎
Corresponding author.
E-mail address: apourlis@vet.uth.gr.

https://doi.org/10.1016/j.smallrumres.2019.10.010
Received 17 March 2019; Received in revised form 4 October 2019; Accepted 26 October 2019
Available online 09 November 2019
0921-4488/ © 2019 Elsevier B.V. All rights reserved.
A. Pourlis
Fig. 1. The anatomy of small ruminant mammary gland and the morphology of alveoli with the characteristic secretory epithelium (adapted and modified from
Barone, 2001).
plays an important role in maintaining the udder tightly attached to the
ventral abdominal wall. Each half udder (Fig. 1) shows internally a
typical tubulo-alveolar structure with a big cistern (sinus lactiferus),
divided in two parts: glandular cistern (sinus lactiferous pars glandularis)
and teat cistern (sinus lactiferous pars papillaris). The cisterns are sepa-
rated by a bundle of smooth muscular fibers, traditionally known as the
cricoid fold, important for the milk drainage. This also helps to keep the
teat and gland morphology divided during machine milking to avoid
the appearance of cluster climbing. Size and form of the gland cistern
vary according to the breed and milking ability of the sheep, being
greater and plurilocular in high yielding ewes. Another sphincter with
smooth muscular fibers is present around the streak canal (ductus pa-
pilaris) in the distal part of the teat, connected to the exterior by a
unique orifice (ostium papilare) (Turner, 1952; Ruberte et al., 1994; Caja
et al., 2000; Rovai et al., 2004).
The mammary gland consists of two main histological structures:
the parenchyma and the stroma (Lérias et al., 2013). The ultimate
mammary gland structures in the parenchyma are the secretory lobes,
consisting of much branched intralobular ducts and alveoli (Suarez and
Morujo, 1982). The alveolus is the secretory unit of the mammary
gland; it consists of specialised cubic epithelial cells (lactocytes) with a
cavity (the lumen), into which the milk is stored after secretion (Fig. 1).
Although Turner (1952) has provided some information on the
structure of the epithelia of the cisterns, these were not detailed. The
few microscopical studies of the ovine mammary gland have been
confined to the alveolar secretory tissue. In the teat and lactiferous si-
nuses of the ovine mammary gland, most of the epithelial lining is
composed of a double layer of non-secretory cells (Brooker, 1984). The
basal layer consisted of flattened cells, whereas, in the superficial layer,
the cells were cuboidal or columnar in shape, depending on the state of
distension of the sinus. Macrophages and lymphocytes are present in
both layers of the epithelium. A marked feature of some non-secretory
cells in the lactiferous cistern and large ducts was a single cilium up to
4 μm long. The presence of such large numbers of ciliated cells is found
only in ewes. Ciliated cells were also present in the teat cistern, but in
small numbers. In addition to non-secretory cells, the epithelial lining
of the lactiferous cistern and large ducts contained large numbers of
cells, of which the ultrastructural features were identical to those of
nearby secretory cells forming the alveoli of the mammary gland
proper. The ability of sheep mammary glands to produce milk is de-
termined by the number of cells secreting milk and their level of ac-
tivity. Changes in the number of cells in the udder occur during the
lactation period. During early and mid-lactation, there was an incre-
ment of alveolar numbers, size and differentiation, as well as the pre-
sence of epithelial cells with a columnar shape and secretory vesicles. It
has been shown that mammary cells proliferate during this process,
while other cells die through apoptosis. The decline in milk production
after peak lactation appears to be due to a gradual reduction in the
number of milk-secreting cells, either through cell death or by the
abrasion of epithelial cells during milk ejection (Boutinaud et al.,
2
Small Ruminant Research 184 (2020) 106009
2004).
Mammary epithelium and stroma communicate with each other and
stromal derived factors influence the activities of mammary epithelium,
although it is not known how the connective tissue mediates paracrine
effects in secretory cells (Colitti et al., 2005).
3. Methods for evaluating udder morphology
3.1. Udder typology
The anatomical characteristics of the mammary gland of ewes are
important for milk production and the aptitude of the udder to milking.
In order to study the udder traits of the sheep, numerous relevant
studies have been performed (Supplementary Material 1). Two main
modes to appraise the external udder morphology can be distinguished:
measurements or scoring. However, in dairy research, these procedures
have been evolved and adopted mainly to machine milking. Both have
been employed in combination or individually.
The relationship between udder type and milkability was estimated
in an experimental flock of Assaf (Awassi × East Friesian) breed ewes
by Sagi and Morag (1974). The authors established the first outlines of
ovine udder conformation and introduced the first method of udder
scoring known as typology. The udders were classified into four types
on the basis of external appearance. In type I, the teats were high up
and showed no differentiation between left and right glands. In type II,
the teats were at a similar height but with a slight differentiation be-
tween the glands. In type III, the teats were lower and the glands were
clearly divided. In type IV, the teats pointed downwards and the glands
were clearly divided (Sagi and Morag, 1974). Later, Jatsch and Sagi
(1979) described an additional type (V) characterized by non-symme-
trical udder halves (Fig. 2).
Gootwine et al. (1980) adopted a different methodology. The udder
conformation of Assaf breed was characterized by four sub-traits, spe-
cifically udder shape, teat location, teat length and teat thickness. Each
sub-trait was rated with four scores; a comparison of these typologies is
in Fig. 2.
Labussière et al. (1981) provided an extensive set of qualitative and
quantitative data on the udder morphology of Lacaune ewes. In parti-
cular, the authors recorded the position of the teats with five scores and
measured udder depth, udder volume, back surface of the udder, teat
length and width (diameter), cistern height and teat inclination (Fig. 3).
This was the first assessment of udder morphology using the combi-
nation of measurements and scoring.
An important advancement of the study of udder morphology in
relation to milkability was accomplished in an extensive project for the
evaluation of the udder in Mediterranean sheep breeds. The metho-
dology used was that of Labussière (1981). In this context, the udder
morphology of Lacaune, Sarde, Manchega, Tsigaya, Churra, Serra de
Estalla and Karagouniko breed was assessed (Labussière, 1988). Further
methodologies for morphological evaluation of ewes udder were
A. Pourlis
Fig. 2. Udder typology of various sheep breeds (adapted from Rovai et al., 2004).
applied by Mavrogenis et al. (1988); Portolano et al. (1999) and
Milerski et al. (2006) (Fig. 3).
3.2. Udder linear scoring
Application of a system for morphological appraisal of the udder
using a linear scale has been proposed for dairy ewes, as an alternative
to the classification by types and the Labussière methodology (de la
Fuente et al., 1996). The evaluation method proposed has been based
on scoring four basic udder traits and a fifth trait that globally defines
udder morphology, on a nine-point linear scale (Fig. 4). The five traits
have been associated with aptitude for machine-milking. Scores for
udder depth, udder attachment, teat position-placement, teat size and
udder shape were assigned at the same time as those for the linear body
conformation traits. The first four udder traits are single linear traits,
and the last, udder shape, is a composite trait defined as the morpho-
logical adaptation of the entire udder for mechanical milking. The
maximum score for this composite trait was 9 (de la Fuente et al.,
2011).
Udder depth was defined by the distance between rear attachment
and the udder floor, using as a reference the hock. Udders with ex-
cessive depth (below the hock) usually reflect deficiencies in the sus-
pensory ligament. Udder attachment was determined by the perimeter
of the insertion to the abdominal wall of the ewe. The maximum in-
sertion base (score = 9) is considered optimum. Teat placement is de-
fined by teat angle. The optimum is completely vertical teats
(score = 9), directed towards the ground, that coincide with minimum
cistern height. Teat size is determined by length. Udder shape measures
the morphology of the udder relative to the optimum for machine
milking (score = 9) and corresponds to the ‘udder machine’ described
by Mikus (1978).
The method of de la Fuente et al. (1996) is the Spanish version of
linear scoring of the sheep udder and applied to Spanish breeds
(Fernández, Baro et al., 1997; Serrano et al., 2002; Legarra and Ugarte,
2005). Later, two more scoring approaches have developed in Italy and
3
Small Ruminant Research 184 (2020) 106009
France, based on already existing models (Fig. 4). Two relevant ap-
praisal tables, both based on 9 point scales per trait, were similar with
only slight differences (Marie-Etancelin et al., 2001).
In the French model, distance of udder lower surface from hocks
(which takes into account differences in animal size), teat position (TP)
(which considers the right teat angle from the vertical line), udder cleft
(UC) degree of separation of the two halves, appraised as combination
of the angle and the height of the cleft, expression of the strength of the
suspensory ligament. Udder Attachment (UA) ratio between the width
and the depth of the udder.
The Italian model (Casu et al., 2006) takes into account four udder
traits (Fig. 4), each scored on a 9-point linear scale: teat placement (TP),
udder depth (UD), degree of separation of the two halves (DS) and
degree of suspension of the udder (SU). For teat placement, the distance
between the teats and the lower surafce of the udder is taken into ac-
count. Scores range from 1, for teats placed on the lowest part of the
udder, to 9, for teats located above the area with the maximum radius
of curvature.
Udder depth is the distance between the udder cleft and the ab-
dominal wall, taking as a reference point the line joining the hocks. It is
scored from 1, for deep udders in contact to the ground to 5, for clefts at
the hock level, to 9, for shallow udders close to the abdominal wall.
The SU is the ratio between the udder attachment width and udder
height. Is is scored from 1, for udders with an attachment width much
smaller than the UD, to 7, for square udders, to 9, for udders with at-
tachment width much larger than the UD. In a Spanish model (de la
Fuente et al., 1996), the SU is not scored directly, but may be calculated
by combining the udder attachment score (i.e., the perimeter of udder
insertion on the abdominal wall) and the UD score.
Finally, DS scores the strength of the median ligament, from 1, with
no separation between the left and right glands, to 9, for udders clearly
divided into two halves.
A. Pourlis
3.3. Ultrasonographic evaluation
The ultrasonography of the ovine udder has been reviewed by
Barbagianni et al. (2017). Bruckmaier and Blum (1992) have first in-
troduced udder ultrasonographic evaluation in ewes. Later, Ruberte
et al. (1994) have employed ultrasonographic evaluation to study the
principal internal structures of the entire ovine udder. Ruberte et al.
(1994) have thus examined the udders of Ripolessa ewes. Mammary
cistern anatomy derived from ultrasonographic measurements and
milking characteristics with and without manual pre-stimulation in
early (2nd – 4th month) or late (5th – 8th month) lactation period were
described in Lacaune and East Friesian dairy ewes (Bruckmaier et al.,
1997). The use of linear measurements taken directly from ultrasono-
graphic images to estimate cistern size in dairy Sarda ewes was assessed
4
Small Ruminant Research 184 (2020) 106009
Fig. 3. Chart for performing linear measure-
ments in ewes’ udder (Labussière et al., 1981;
Portolano et al., 1999; Milerski et al., 2006).
Sources:
Labussière et al. (1981): P = udder depth.
Portolano et al. (1999): c at = circumference
at the site of attachment, c max = maximum
circumference, hm = udder height, lm= udder
width, lnt = teat length, lgt = teat diameter, αd
= teat angle, hc = cistern height, prof = udder
depth, Jar = distance between the teat and the
hock, Isc = distance between the ischium and
the site of udder attachment.
Milerski et al. (2006): A = udder length, B =
udder width, C = rear udder depth, D = cis-
tern depth, E = teat length, a = teat angle.
(Nudda et al., 2000). Ultrasonographic examination has been used to
evaluate cisternal size changes when different milking intervals have
been performed in dairy ewes (Castillo et al., 2008). The objective of
another study was to analyze differences in milk partitioning, between
the udder compartments (cisternal and alveolar) of two dairy sheep
breeds (Manchega and Lacaune), of different genetic merit and milk
yield to understand the differences observed in daily milk secretion and
milking ability (Rovai et al., 2008). Makovicky et al. (2015a, 2015b)
studied the size of mammary cistern in ewes of nine genotypes.
3.4. Digital image analysis
New perspectives to appraise traits related to the milkability of
dairy ewes, in particular udder morphology and the kinetics of milk
A. Pourlis Small Ruminant Research 184 (2020) 106009

Fig. 4. Linear scoring scales of ovine udder.

Fig. 5. Use of digital pictures to obtain udder measurements (Adapted from Marie-Etancelin et al., 2003).

5
A. Pourlis
emission, were employed using digital pictures and software of image
analysis (Marie-Etancelin et al., 2003). The implementation of digital
picture analysis for the measurements of udder morphology allows the
extraction and calculation of measurements from a digital picture.
Three pictures of the udder were analysed: fore and lateral views of the
whole udder and a particular view of the right teat. An issue with the
method is the necessity to include a set of many different measurements
(Fig. 5).
4. Associations of the udder morphological traits
4.1. Associations with milk production
Supplementary Material 2 and 3 summarize the linear measure-
ments of udder and teat traits in various ovine breeds. The linear
scoring of udders can be found in Supplementary Material 4. Indicative
correlations of udder traits with milk yield are depicted in
Supplementary Material 5.
Positive and significant correlations were observed between milk
yield and udder volume in Sicilo-Sarde dairy sheep (Ayadi et al., 2011).
Correlation between cisternal milk and cisternal area was positive but
moderate, as was the correlation between cisternal area and estimated
daily milk yield. According to the authors, the Sicilo-Sarde breed
showed adequate udder morphology for machine milking (Ayadi et al.,
2011). Milk yield in Najdi sheep was positively correlated with udder
depth, width, circumference and distance between teats (Ayadi et al.,
2014). In the Australian Merinos (Bencini and Purvis, 1990), udder
volume and milk yield in the first nine weeks of lactation were sig-
nificantly correlated.
In both genotypes (Awassi, East Friesian X Awassi) phenotypic re-
lations between UH (udder height from ground), TD (teat distance), UV
(udder volume) and 60, 90, l20-day milk yields and total milk yield was
relatively high and significant (Şeker et al., 2004). Correlation between
UH and milk yield was negative while it was positive between TD, UV
and milk yields. In Awassi ewes, significant phenotypic relations were
determined between UD (udder depth) of day 120 and l20 day milk
yield, UD of day 90 and day I20 and total milk yield. In crossbreeds, UD
values measured on days 90 and 120 were correlated to total milk yield.
Significant phenotypic correlations were found in Awassi ewes between
udder circumference (UC) of day 60 and 60-day milk yield, and be-
tween those of 60 and I20 days and total rnilk yield. No significant
relationship was found between right teat length (RTL) and milk yields
in Awassi. However, in crossbreeds, phenotypic correlations were sig-
nificant between RTL of days 60 and 60 day milk yield, RTL of day 90
and l20 day and total milk yield. Significant phenotypic relations be-
tween the diameter of the right teat (DRT) of day 60 and 60-day milk
yield were found in Awassi ewes. These correlations were observed in
crossbreed ewes between DRT of day 60 and 60 day milk yield and DRT
of day 60 and day 90 and 90-day milk yield. In this study, a negative
correlation between UH and milk yield at various periods of the lac-
tation and positive correlation between TD, UD, UV and milk yield at
various days of the lactation were found. Those udder-teat traits have a
potential to be employed for selection of breeder animals for milk
production in either Awassi or crossbreed ewes (Şeker et al., 2004).
Iñiquez et al. (2009) performed a study in two Awassi sheep genotypes
and their crosses in order to assess the values of different udder mea-
surements for predicting milk production traits. Udder circumference
and width and teat width and position had greater correlations with
milk yield on d 70 and total milk yield (r = 0.49 to 0.80) than did other
measurements. Udder circumference and teat width have been shown
to be significantly correlated with total milk yield. Correlation was
strong and significant between udder circumference and width
(r = 0.96). Thus, udder circumference and teat width appear to be the
most useful of the udder measurements taken for predicting total milk
yield of Awassi sheep. A medium to strong correlation was found be-
tween average teat position score with milk yield on d 70 of lactation.
6
Small Ruminant Research 184 (2020) 106009
An additional measurement with some ability for predicting production
traits was cistern height although this negatively correlated with milk
yield on d 70. Measurements that displayed low correlations with milk
yield and other production traits included udder height, udder length,
and teat length, making them unsuitable for predicting milk production
performance (Iñiquez et al., 2009).
Positive correlations (P < 0.05, P < 0.001) were observed be-
tween all udder traits and daily milk yield in Bafra ewes. Conversely,
negative correlations were obtained between teat-floor distance and
daily milk yield. Teat traits did not show any significant correlation
with daily milk yield except between teat distance and daily milk yield
within the range of 0.302-0.605 (P < 0.05). Length and diameter of
teats were not significantly correlated with milk flow rate (MFR) and
milking duration (MD) (P > 0.05), while udder depths were sig-
nificantly correlated with MFR (Ünal et al., 2008).
Positive and significant correlations (P < 0.01) were observed be-
tween udder circumference and udder width and daily milk yield in
Bandirma sheep. Therefore selection to improve any one of these traits
might lead to an improvement of the others (Sezenler et al., 2016).
Correlation between cisternal area and cisternal milk volume was
r = 0.79 (P < 0.05), and breed differences (Lacaune versus Manchega)
were reported. The lower correlation coefficient observed for Lacaune
ewes, whose volume of cisternal milk was significantly greater, was
probably due to the size limitations for visualizing the entire cisternal
area when using a 5-MHz ultrasound transducer. The positive re-
lationship found between the area of udder cisterns by ultrasonography
and the amount of milk produced in both breeds leads to consider this
method as a useful tool for evaluating the capacity of the sheep udder
(Rovai et al., 2008). Correlations between morphological udder traits
and milk yield were positive and significant (r = 0.44–0.65; P < 0.05)
in both breeds, showing that milk yield was related to udder size (Rovai
et al., 2008).
Teat length of Istrian dairy crossbreed ewes did not show any cor-
relation either with other milking or morphological characteristics.
Positive and significant correlations were also observed between udder
volume and all milking characteristics. Teat angle was also negatively
and significantly correlated with milk yield and milking time (Dzidic
et al., 2004).
In the Mehraban breed, the largest correlation coefficient was found
between udder circumference at two weeks post-weaning with lactation
yield. In Ghezel, correlation coefficients of lactation yield with udder
measurements at two weeks post-weaning were not significant
(Izadifard and Zamiri, 1997). However, at two weeks postpartum,
several udder measurements were highly correlated with the lactation
yield; the largest correlation coefficients were noted with the right
udder depth and udder circumference. The results of the present ex-
periment showed that milk potential of mature Ghezel ewes can be
estimated with reasonable accuracy by measuring udder depth and
length around peak of lactation. While udder depth and length at two
weeks postpartum accounted for 72% of the variation in milk yield of
Ghezel ewes, udder circumference at two weeks after weaning ex-
plained about 46% of the variation in milk yield of the Mehraban breed.
The accuracy was greatest when the amount of harvested milk during
the suckling period was included as a parameter of yield estimation. For
practical purposes, Izadifard and Zamiri suggested udder measurements
around peak of lactation in Ghezel, and the harvested milk during the
last month of the 15-week suckling period for estimation of the milk
potential in both breeds (Izadifard and Zamiri, 1997).
A significant correlation between all udder linear scores of Lori
Bakhtiari ewes with daily milk yield was found; udder depth was highly
correlated with daily milk (Sadeghi et al., 2013).
Chios ewes with udders classified as ‘defined halving’ and ‘too flat’
produced significantly more milk than ewes with ‘broken’ or asym-
metric udders (Mavrogenis et al., 1988). Moderate to high were the
correlations of udder depth with udder floor, udder quality, udder
circumference and milk production. Udder circumference before
A. Pourlis
milking was positively and highly correlated with test-day, 90-day and
total milk yield. Teat length was highly correlated with teat diameter,
but relationships between teat measures and milk production were
generally low, while those between teat measures and qualitative and
quantitative udder characteristics were low to moderate (Mavrogenis
et al., 1988). Phenotypic correlations among udder floor, udder quality,
milking ease and other traits were variable in sign, but were all very
low and insignificant. Udder circumference was positively correlated
with udder depth and milk production (Mavrogenis et al., 1988).
McKusick et al. (1999) studied the effects of udder morphology on
commercial milk production of East Friesian crossbred ewes. It was
estimated that for each cm increase in udder circumference and udder
height, there was a relative increase of 0.06 and 0.11 litres respectively
of daily commercial milk yield. In the same experiment, for each cm
increase in cistern height there was a relative increase of 0.12% units of
milk fat.
At 2 weeks post-partum, the correlation of milk yield of Kermani fat
tail sheep with udder circumference and udder width was significant
(Kahtuei et al., 2008).
4.2. Associations in animal selection
Supplementary Material 5 and 6 show the repeatabilities and her-
itabilities of udder traits, respectively in various breeds. The repeat-
ability and heritability of morphological charactersistcs of the udder
and their releations with milk production and milking time are essential
in programs of improvement of animals in terms of udder morphology
(Rovai et al., 2004). The values of linear scores calculated by
Fernández, Baro et al. (1997) in Churra ewes were found to be re-
peatable (r = 0.48–0.64) and showed low heritability values
(h2 = 0.16–0.24). All heritability estimates were moderate to high
(0.27 to 0.83), except for udder floor (0.18) in Chios ewes (Mavrogenis
et al., 1988). Heritabilities of udder traits reported in Assaf (h2 = 0.23
to 0.42) (Gootwine et al., 1980) were moderate. The same general
findings appeared in Sarda ewes (h2 = 0.27 to 0.37) (Carta et al., 2001;
Casu et al., 2006). However, increased heritability values were obtained
from Sarda × Lacaune backcross ewes and daughters and grand-
daughters sired by Sarda rams (Casu et al., 2010). The values of udder
measurements were generally highly repeatable in Awassi, Chios and
Churra ewes. Also, high repeatabilities were shown from the linear
udder traits of various dairy breeds (r = 0.41–0.73) (Table 5). How-
ever, in Manchega breed, the linear udder traits were the smallest
(r = 0.26–0.47) (Serrano et al., 2002).
The traits of Churra ewes related to udder size (depth, width, cir-
cumference) were significantly influenced by lactation month, flock and
milk yield and showed low repeatability (0.17 – 0.18). The traits related
to cistern morphology (cistern height, teat position, angle) were sig-
nificantly influenced by flock and parity number. These traits, together
with teat length and width, had high repeatabilities (0.45 - 0.77)
(Fernández et al., 1995). With regard to linear udder traits of Churra
ewes, the highest heritability values were obtained for udder depth
(0.26) and teat placement (0.22) and the lowest for udder attachment
(0.09); udder shape and teat length had values of 0.15 and 0.16 re-
spectively (de la Fuente et al., 2011).
4.3. Associations with milkability
Machine-milkability is normally estimated by fractional miking or
by analysis of milk emission curves obtained during machnine- milking
without extrastimulation of the mammary gland (Caja et al., 2000;
Marie-Etancelin et al., 2001).
Before proceeding with aspects of udder morphology and milk-
ability, notice should be taken to some anatomical peculiarities of the
sheep. Within the most ventral (and to some degree, lateral) aspect of
the udder, lies a compartment known as the gland cistern, that in-
corporates a tortuous system of cavities into which the large lactiferous
7
Small Ruminant Research 184 (2020) 106009
ducts empty. The second important compartment of the udder, located
more medially, is the alveolar region that is rich with milk secreting
epithelium and small interlobular ducts (Marnet and McKusick, 2001).
Sheep have proportionally larger cisterns (40–80% of the total volume).
These larger cisterns play an important role in storage of milk between
milkings and can greatly affect the removal of milk at the time of
milking (Marnet and McKusick, 2001). Therefore, the partitioning of
milk within the mammary gland, in particular the proportion of cis-
ternal milk volume, relative to the total volume obtained after a normal
milk ejection reflex, would appear to be perhaps a better indicator of
the adaptation of the animal to machine milking.
Sagi and Morag (1974) were the first to suggest that the pattern of
milk fractions could be related to udder conformation: indeed, they
found a higher percentage of machine produced milk in the udder with
teats pointed downwards and glands clearly divided, compared to
udder with teats implanted high and no differentiation between the two
halves. In the Sarda ewes, Casu et al. (1983) found positive correlations
for the volumes of machine- or hand-strippings with height of the cis-
tern (0.53 and 0.58), inclination of teats respect to the vertical axis
(0.50 and 0.52) and teat position with respect to the fore-rear axis (0.47
and 0.58). Milk fractions collected during milking (machine milk and
stripping milk), residual milk (obtained after oxytocin injection) and
milk flow curves during machine milking were used to evaluate ma-
chine milking ability in dairy sheep (Labussière, 1988; Caja et al.,
2000). Moreover, milk partitioning between cisternal and alveolar
compartments may influence milk secretion and milk yield response to
extended milking intervals (Castillo et al., 2008). Large differences
between breeds exist with regard to the proportion of total milk that
can be stored within the cisternal compartment (Bruckmaier and Blum,
1992). In sheep, high variation in cisternal milk was reported, ranging
from < 30% for meat-type breeds (Caja et al., 1999) to > 50% for dairy
breeds (Caja et al., 2000; Nudda et al., 2000; McKusick et al., 2002),
suggesting that selection for greater milk yield also resulted in larger
cisternal udders to accommodate the greater milk volumes secreted
(Rovai et al., 2008).
Sheep breeds differ in udder conformation and this makes the de-
velopment of optimal mechanical milking equipment more difficult. In
machine-milked sheep, a relatively larger proportion of milk yield is
obtained as ‘stripping’ milk (Labussière, 1988) and in milking parlours
this can result in a 42% reduction in the number of animals milked per
hour (Fernández et al., 1989). Some of the machine-milking problems
are actually due to the fact that the design of the systems is based on
Lacaune breed characteristics. Lacaune ewes have more narrow
(15 mm) teats than Churra (16 mm), Karagouniko (17.7 mm), Man-
chega (17.9 mm), Sarda (16 mm), Serra da Estrela (17 mm) and Tsigay
(16.3 mm) ewes (Labussière, 1988). Also in Lacaune ewes, by esti-
mating high phenotypic correlations between total stripping (machine-
and hand-strippings) and scoring of udder depth (-0.75) and teat im-
plantation (0.57), confirmed that its volume increases in long udder
with high implanted teats (Casu et al, 2000).
4.4. Associations with mammary health
According to Legara and Ugarte (2005) the udders must have good
attachment in order to produce enough milk without functional pro-
blems. Big udder depth creates difficulties during milking and presents
bigger probability of injuries (Legara and Ugarte, 2005). Udder shape,
is a composite trait defined as the morphological adaptation of the
entire udder for mechanical milking. The appraisal of udder shape is
not necessary because this trait is the combination of other traits and
there are high genetic correlations among teat position, udder attach-
ment and udder shape (Fernández, Baro et al., 1997; Fernández,
Requena et al., 1997; Serrano et al., 2002). This indicates that the
general and subjective trait is associated with the view of teat position
and udder attachment but not with udder depth and teat size and
consequently does not reflect the global picture of the udder. Teat
A. Pourlis
position is important for the application of milking cups because the
horizontal teats are bending due to the weight of the cups and their fall.
The milking cups have good fit in teats of medium size but not in big or
small (Legarra and Ugarte, 2005). The appraisal of udder depth and teat
size is considered very important because these traits contribute to a
great extent to the seamless implementation of machine milking.
Fernández, Baro et al. (1997) reported that the phenotypic correlations
between the morphological udder traits and the logarithm of somatic
cells indicate that the operations during milking cause possible infec-
tions in the udders which have big depth and big teats. In the majority
of the studies, the teat placement was the trait with the largest genetic
variability, which could be useful in breeding programmes in order to
improve udder suitability to machine -milking (Serrano et al., 2002;
Marie-Etancelin et al., 2005). Oget et al. (2019) summarized few stu-
dies in dairy and meat-producing sheep which dealt with estimating
genetic correlations between udder-type and mastitis-related traits. The
hypothesis of the mammary epithelial cell-producing antibacterial
proteins has been surveyed by Katsafadou et al. (2019). The authors
have noted the significant involvement of ewes’ mammary glands’
structural units in the defensive process against mastitis-causing bac-
teria.
5. Genome scanning - quantitative trait loci
Genome scanning for detection of quantitative trait loci (QTL) is an
efficient approach to identify loci that influence the phenotypic var-
iance of economically interesting traits. Recent studies on the mam-
mary gland related to morphology, refer to the identification of quan-
titative trait loci (QTL) affecting udder traits in dairy sheep (Casu et al.,
2003). These authors have been working in QTL detection with the
hypothesis of the presence of different alleles controlling udder mor-
phology on a population of F1 crossbred Lacaune and Sarda ewes (Carta
et al., 2002). Several QTL affecting udder morphology traits were de-
tected for the first time through methods consisting of extracting ob-
jective measurements from digital pictures and repeated udder scoring.
QTL for udder traits have been reported in the Sarda × Lacaune po-
pulation, the Lacaune - Manech families (Barillet et al., 2006) and in
Churra ewes (Gutiérrez-Gil et al., 2008).
In the Sarda × Lacaune population, a detailed study of udder mor-
phology traits was performed, with digital picture measures being re-
corded in the cross-bred animals and a large list of udder morphology
related traits being analysed for QTL detection. Genome-wise sig-
nificant QTL were detected in Ovis aries chromosome (OAR): OAR3,
OAR4, OAR9, OAR14, OAR16, OAR20, OAR22 and OAR26. In the
Lacaune-Manech population, genome-wise suggestive QTL were iden-
tified in OAR6 and OAR17 chromosomes for udder cleft (Barillet et al.,
2006). In the same population, QTL were also detected for traits related
to the kinetics of milk emission, which are directly related to the ma-
chine-milking ability of the ewes. The difficulties to measure these traits
in commercial populations make such analyses of great value for the
sheep research community. Genome-wise suggestive QTL for these
traits were detected on OAR9, OAR11, OAR15, OAR17 and OAR20,
with the most significant QTL influencing maximum milk emission flow
on OAR11. In the commercial population of Spanish Churra sheep, a
genome scan for udder morphology traits assessed according to the 9-
point linear scale described by de la Fuente et al. (1996) identified
chromosome-wise significant QTL on OAR7, OAR14, OAR15, OAR20
and OAR26. The most significant of these QTL was that identified in the
proximal end of OAR7 for teat placement (Gutiérrez-Gil et al., 2008).
6. Concluding remarks
In the present review, numerous research articles have been sur-
veyed in order to collect morphological data of udder traits and to as-
semble a picture about the ovine udder morphology and the associa-
tions with milk production. Despite the wealth of data, these
8
Small Ruminant Research 184 (2020) 106009
information are not homogenous in order to compare and extrapolate
easy and definite deductions. The studies which employed measure-
ments did not allow authors to compare breeds and to estimate genetic
parameters due to small amount of ewes often measured in different
environments. However, some authors estimated average to high her-
itabilities of some morphological udder and teat traits. When these
traits are related to milk yield the greatest effects are observed for the
udder width and height (also called depth). Main effects of teat traits
are related to milk emission during milking.
The typology of the udders despite the small scale implementation,
showed a close relationship with milkability. Typology is recommended
as a useful tool for the screening of animals, for example, in order to
standardize groups for machine milking.
The linear scoring has been used widely in large scale researches.
The values of linear scores were sufficiently repeatable and showed
intermediate heritability. Nevertheless, udder shape showed high and
positive genetic correlation with udder attachment and teat placement,
as a result of the main role of these traits in the definition of udder
shape. Consequently, the use of the first four linear udder traits will be
sufficient to improve programs of udder morphology. Phenotypic and
genetic correlations showed that selection for milk yield will produce a
worse udder morphology, mainly in udder height and teat placement,
giving as a result baggy udders which are inadequate for machine-
milking.
Mammary ultrasonography is an efficient method to evaluate the
size and the productive capacity of the ovine udder. Cistern height and
teat position, angle, length and width determine the morphological
aptitude of the udder to mechanical milking and, moreover show high
repeatability. Thus, these traits may be suitable selection markers to
improve milking ability.
In order to obtain a seamless implementation of mechanical
milking, the udders must be uniform and must bear the characteristics
of the “perfect udder”. The assessment of the morphological udder traits
during milking is important for a positive progression in genetic im-
provement related to the ability and adaptability in the mechanical
milking of dairy ewes. Due to the fact that the morphological and
anatomical traits of the udder are considered important both for the
milk production and the milkability of the animals, the research must
continue. The research should be performed with an integrated and
uniform methodology. The advancement of research should focus at the
relation of the udder morphology with the milk kinetics, composition
and hygiene. The problem of correlation between mammary gland
morphology and mammary gland health has not received much atten-
tion in sheep breeding, as indicated by the lack of literature on this
subject.
In this way, the investigations could approach the ultimate target:
proper and uniform udders, very good milkability and superior milk
quality.
Conflict of interest
The Author does not have any conflict of interest
Appendix A. Supplementary data
Supplementary material related to this article can be found, in the
online version, at doi:https://doi.org/10.1016/j.smallrumres.2019.10.
010.
References
Ayadi, M., Such, X., Ezzehizi, N., Zouari, M., Najar, T., Ben, M., Rad, M., Casals, R., 2011.
Relationship between mammary morphology traits and milk yield of sicilo-sarde
dairy sheep in Tunisia. Small Rum. Res 96, 41–45.
Ayadi, M., Matar, A.M., Aljumaah, R.S., Alshaikh, M.A., Abouheif, M.A., 2014. Evolution
of udder morphology, alveolar and cisternal milk compartment during lactation and
their relationship with milk yield in najdi sheep. Span, J. Agric. Res. 12, 1061–1070.
A. Pourlis
Barbagianni, M.S., Mavrogianni, V.S., Vasileiou, N.G.C., Fthenakis, G.C., Petridis, I.G.,
2017. Ultrasonographic examination of the udder in sheep. Small Rum. Res. 152,
86–99.
Barillet, F., Arranz, J.J., Carta, A., Jacquiet, P., Stear, M., Bishop, S., 2006. Final
Consolidated Report of the European Union Contract of Acronym “genesheepsafety”
(QLK5-CT-2000-00656). pp. 145.
Barone, R., 2001. Anatomie Comparée Des Mammifères Domestiques. Tome 4,
Splachnologie II, Vigot Paris.
Bencini, R., Purvis, I.W., 1990. The yield and composition of milk from merino sheep.
Proc. Aust. Soc. Anim. Prod. 18, 144–147.
Boutinaud, M., Guinard-Flament, J., Jammes, H., 2004. The number and activity of
mammary epithelial cells, determining factors for milk production. Reprod. Nutr.
Dev. 44, 499–508.
Brooker, B.E., 1984. An ultrastructural study of the sinus epithelium in the mammary
gland of the lactating ewe. J. Anat. 138, 287–296.
Bruckmaier, R.M., Blum, J.W., 1992. B mode ultrasonography of mammary glands of
cows, goats and sheep during αand βadrenergic agonist and oxytocin administration.
J. Dairy Res. 59, 151–159.
Bruckmaier, R.M., Paul, G., Mayer, H., Schams, D., 1997. Machine milking of ost friesian
and lacaune dairy sheep: udder anatomy, milk ejection and milking characteristics. J.
Dairy Res. 64, 163–172.
Caja, G., Such, X., Rovai, Maristella, 2000. Udder morphology and machine milking
ability in dairy sheep. Proceedings of the 6th Great Lakes Dairy Sheep Symposium, 2-
4 November, 2000. pp. 25–48 Ontario, Canada.
Carta, A., Barillet, F., Allain, D., Amigues, Y., Bibé, B., Bodin, L., Casu, S., Cribiu, E., Elsen,
J.M., Fraghi, A., Gruner, L., Jacquiet, P., Ligios, S., Marie-Etancelin, C., Mura, L.,
Piredda, G., Rupp, R., Sanna, S.R., Scala, A., Schibler, L., 2002. QTL detection with
genetic markers in a dairy sheep backross sarda X lacaune resource population. 7th
World Congress on Genetics Applied to Livestock Production, August 19-23, 2002.
Montpellier, France.
Carta, A., Casu, S., Salaris, S., 2009. Current state of genetic improvement in dairy sheep.
J. Dairy Sci. 92, 5814–5833.
Carta, A., Casu, S., Sanna, S.R., 2001. Genetic aspects of udder morphology in the sarda
breed: relationships with milk yield. Proc. of the 14th A.S.P.A. Congress, Firenze. pp.
7–9 2001.
Castillo, V., Such, X., Caja, G., Salama, A.A.K., Albanell, E., Casals, R., 2008. Changes in
alveolar and cisternal compartments induced by milking interval in the udder of
dairy ewes. J. Dairy Sci. 91, 3403–3411.
Casu, S., Carta, R., Ruda, G., 1983. Morphologie de la mamelle et aptitude a la traite
mecanique de la brebis sarde. In: Proceedings of the 3rd International Symposium on
Machine Milking of Small Ruminants. pp. 592–603 Sever-Cuesta, Valladolid, Spain.
Casu, S., Marie-Etancelin, C., Schibler, L., Cribiu, E., Mura, L., Fraghi, A., Barillet, F.,
Carta, A., 2003. A Genome Scan to Identify Quantitative Trait Loci Affecting Udder
Morphology Traits in Dairy Sheep. International Workshop on Major Genes and QTL
in sheep and goats, Toulouse, France.
Casu, S., Pernazza, I., Carta, A., 2006. Feasibility of a linear scoring method of udder
morphology for the selection scheme of Sardinian sheep. J. Dairy Sci. 89, 2200–2209.
Casu, S., Sechi, S., Salaris, S.L., Carta, A., 2010. Phenotypic and genetic relationships
between udder morphology and udder health in dairy ewes. Small Rum. Res. 88,
77–83.
Colitti, M., Stradaioli, G., Stefanon, B., 2005. Mammary cell turnover in lactating ewes is
modulated by changes of energy fuels. Res. Vet. Sci. 78, 53–59.
Dzidic, A., Kaps, M., Bruckmaier, R.M., 2004. Machine milking of istrian dairy crossbreed
ewes: udder morphology and milking characteristics. Small Rum. Res. 55, 183–189.
Fernández, N., Joy, S., Torres, A., Molina, P., Peris, C., Rodríguez, M., Gallego, L., 1989.
Sistema de ordeño mecánico en rebaños ovinos lecheros de raza manchega. IV
International Symposium on Machine Milking in Small Ruminants Tel-Aviv, Israel.
pp. 252–271.
Fernández, G., Alvarez, P., San Primitivo, F., de la Fuente, L.F., 1995. Factors affecting
variation of udder traits of dairy ewes. J. Dairy Sci. 78, 842–849.
Fernández, G., Baro, G.A., de la Fuente, L.F., San Primitivo, F., 1997. Genetic parameters
for linear udder traits of dairy ewes. J. Dairy Sci. 80, 601–605.
Fernández, N., Requena, R., Beltran, M.C., Peris, C., Rodríguez, M., Molina, P., Torres, A.,
1997. Comparison of different machine milking clusters on dairy ewes with large size
teats. Ann. Zootech. 46, 207–218.
de la Fuente, L.F., Fernández, G., San Primitivo, F., 1996. A linear evaluation system for
udder traits of dairy ewes. Livest. Prod. Sci. 45, 171–178.
de la Fuente, L.F., Gonzalo, C., Sánchez, J.P., Rodriguez, R., Carriedo, J.A., San Primitivo,
F., 2011. Genetic parameters of the linear body conformation traits and genetic
correlations with udder traits, milk yield and composition, and somatic cell count in
dairy ewes. Can. J. Anim. Sci. 91, 585–591.
Gootwine, E., Alef, B., Gadeesh, S., 1980. Udder conformation and its heritability in the
assaf (awassi X East friesian) cross of dairy sheep in Israel. Ann. Génét. Sél. Anim 12,
9–13.
Gutiérrez-Gil, B., El-Zarei, M.F., Alvarez, L., Bayón, Y., de la Fuente, L.F., San Primitivo,
F., Arranz, J.J., 2008. Quantitative trait loci underlying udder morphology traits in
dairy sheep. J. Dairy Sci. 91, 3672–3681.
Iñiquez, L., Hilali, M., Thomas, D.L., Jesry, G., 2009. Udder measurements and milk
production in two awassi sheep genotypes and their crosses. J. Dairy Sci. 92,
4613–4620.
Izadifard, J., Zamiri, M.J., 1997. Lactation performance of two Iranian fat-tailed sheep
breeds. Small Rum. Res. 24, 69–76.
Jatsch, O., Sagi, R., 1979. Machine milkability as related to dairy yield and its fractions in
dairy ewes. Ann. Zootech. 28, 251–260.
Small Ruminant Research 184 (2020) 106009
Kahtuei, R.M., Shahneh, A.Z., Sharebabak, M.M., 2008. Lactation performance and
suckling lamb growth of kermani fat-tailed ewe. J. Anim. Vet. Adv. 7, 1575–1578.
Katsafadou, A.I., Vasileiou, N.G.C., Fthenakis, G.C., 2019. Use of proteomics in the study
of mastitis in ewes. Pathogens 8, 134.
Labussière, J., 1988. Review of physiological and anatomical factors influencing the
milking ability of ewes and the organization of milking. Livest. Prod. Sci. 18,
253–274.
Labussière, J., Dotchewski, D., Combaud, J.F., 1981. Charactéristiques morphologiques
de la mamelle des brebis lacaune. Méthodologie pour l’obtention des données.
Relations avec l’aptitude à la traite. Ann. Zootech. 30, 115–136.
Legarra, A., Ugarte, E., 2005. Genetic parameters of udder traits, somatic cell score, and
milk yield in latxa sheep. J. Dairy Sci. 88, 2238–2245.
Makovický, P., Milerski, M., Margetín, M., Makovický, P., Nagy, M., 2015a. Genetic
parameters for the size of udder cisterns in ewes diagnosed by ultrasonography
among breeds: improved valachian, tsigai, lacaune and their crosses. Arch. Zootec.
68, 403–408.
Makovický, P., Margetín, M., Makovický, P., 2015b. Estimation of udder cistern size in
dairy ewes by ultrasonography. Mijekarstvo 65, 210–218.
Marie-Etancelin, C., Casu, S., Rupp, R., Carta, A., Barillet, F., 2001. New objectives of
selection related to udder health, morphology and milkability in dairy sheep.
Proceedings of the 52nd Annual Meeting of European Association for Animal
Production, Budapest, Hungary. Wageningen Pers, Wageningen, Netherlands, pp.
272–298.
Marie-Etancelin, C., Aurel, M.R., Barillet, F., Jacquin, M., Pailler, F., Porte, D., Casu, S.,
Carta, A., Deiana, S., Tolu, S., 2003. New tools to appraise udder morphology and
milkability in dairy sheep. In: Gabiña, D., Sanna, S. (Eds.), Breeding Programmes for
Improving the Quality and Safety of Products. New Traits, Tools, Rules and
Organization? CIHEAM, Zaragoza, pp. 71–79 (Options Méditerranéennes : Série A.
Séminaires Méditerranéens; n. 55).
Marie-Etancelin, C., Astruc, J.M., Porte, D., Larroque, H., Robert-Granié, C., 2005.
Multiple-trait genetic parameter and genetic evaluation of udder type traits in la-
caune dairy ewes. Livest. Prod. Sci. 97, 211–218.
Marnet, P.G., McKusick, B.C., 2001. Regulation of milk ejection and milkability in small
ruminants. Livest. Prod. Sci. 70, 125–133.
Mavrogenis, A.P., Papachristoforou, C., Lysandrides, P., Roushias, A., 1988.
Environmental and genetic factors affecting udder characters and milk production in
chios sheep. Génét. Sél. Evol. 20, 477–488.
McKusick, B.C., Marnet, P.-G., Berger, Y.M., Thomas, D.L., 1999. Preliminary results:
effects of udder morphology on commercial milk production of East friesian cross-
breed ewes. Proceedings of the 5th Great Lakes Dairy Sheep Symposium. November
4-6, 1999, Brattleboro, Vermont, USA.
Mikus, M., 1978. Study of the mutual relationship between dimensions of the udder with
regard to improvements of sheep for machine milking. In: Proc. 2nd Int. Symp.
Machine Milking Small Ruminants. INRA-ITOVIC, Alghero, Italy pp.102-I 12.
Milerski, M., Margetín, M., Čapistrák, A., Apolen, D., Špánik, J., Orancová, M., 2006.
Relationships between external and internal udder measurements and the linear
scores for udder morphology traits in dairy sheep. Czech J. Anim. Sci. 51, 383–390.
Nudda, A., Pulina, G., Vallebella, R., Bencini, R., Enne, G., 2000. Ultrasound technique for
measuring mammary cistern size of dairy ewes. J. Dairy Res 67, 101–106.
Oget, C., Tosser-Klopp, G., Rupp, R., 2019. Genetic and genomic studies in ovine mastitis.
Small Rum. Res. 176, 55–64.
Portolano, B., Taodaro, M., Finocchiaro, R., Giaccone, P., Pagnacco, G., 1999. Évaluation
par analyse multivariate de la conformation de la mamelle chez la brebis Valle del
belice en relation avec la production laitière. Ann. Zootech. 48, 381–388.
Rovai, M., Thomas, D.L., Berger, Y., Caja, G., 2004. Udder morphology and effects on milk
production and ease of milking in dairy sheep. In: Proceedings of the 10th Great
Lakes Dairy Sheep Symposium. pp. 79–114 November 4-6, 2004, Wisconsin, U.S.A.
Rovai, M., Caja, G., Such, X., 2008. Evaluation of udder cisterns and effects on milk yield
of dairy ewes. J. Dairy Sci. 91, 4622–4629.
Ruberte, J., Carretero, A., Fernández, M., Navarro, M., Caja, G., Kirchner, F., Such, X.,
1994. Ultrasound mammography in the lactating ewe and its correspondence to
anatomical section. Small Rum. Res. 13, 199–204.
Sadeghi, S., Rafat, S.A., Ghaderi Zefrei, M., Khaligh, F., Rostami, K.H., Bohlouli, M.,
Bahrani Behzadi, M.R., Mohaghegh, M., 2013. Factors affecting external and internal
mammary morphology traits and assessment of their interrelationships with milk
yield in Lori bakhtiari breed ewes. Livestock Res. Rural Dev. 25 (3) article 37.
Sagi, R., Morag, M., 1974. Udder conformation, milk yield and fractionation in the dairy
ewe. Ann. Zootech. 23, 185–192.
Şeker, I., Kul, S., Bayraktar, M., Akcan, A., 2004. Effects of crossbreeding with East-
friesian to awassi on milk production and mammary gland traits. Medycyna Wet. 60,
815–818.
Serrano, M., Pérez-Guzman, M.D., Montoro, V., Jurado, J.J., 2002. Genetic analysis of
udder traits in manchega ewes. Livest. Prod. Sci. 77, 355–361.
Sezenler, T., Ceyhan, A., Yüksel, M.A., Önaldi, A.T., Yildirir, M., 2016. Effect of parity and
type of lambing on performance and udder traits of Bandirma ewes. Indian J. Anim.
Sci. 86, 572–577.
Suarez, A.J.A.-M., Morujo, A.A., 1982. Variations in the shape of the mammary gland
alveoli. Anat. Histol. Embryol. 11, 65–75.
Turner, C.W., 1952. The Anatomy of the Udder of Sheep. In: The Anatomy of the
Mammary Gland. Lucas Brothers Publishers, Columbia, Missouri, pp. 315–331.
Ünal, N., Akçapinar, H., Atasoy, F., Yakan, A., Uğurlu, M., 2008. Milk yield and milking
traits measured with different methods in Bafra sheep. Revue Méd. Vét. 159,
494–501.