Productivity and Genetic Potential of Garole Sheep of India-A Review
Uttam Kumar Pal
Sheep are the only domestic animals which can utilize wastelands, stubbles of cultivated corps, tree topping, farm wastes or weeds from the field to convert them into meat, wool and skin. In India sheep contribute greatly to the agrarian economy, especially in the arid/semi-arid and mountainous areas where crop and/or dairy farming are not economical. Garole is a native and local sheep of Bengal in extended costal Sundarban area having distinct and separate phenotypic characters, productive performances of their own and is not thoroughly characterized and established as Breed. This sheep is the latest sensations in the world of domestic species by virtue of its prolificacy, lambing frequency, disease resistance and other extraordinary merits rarely or not even observed in other sheep breeds of the world. The sheep Garole is very popular for its bi-annual lambing, multiple birth, grazing on aquatic weeds and grass in knee-deep water and disease resistance characters. They are small in size; produce rough wool, good quality skin, manure and low fat mutton. Milk is having no importance as the quantity is too less to feed its kids. In this review an attempt has been made to present detail phenotypic and genetic characteristics of Garole in relation to other sheep breeds with emphasis on products characteristics, disease resistance, litter size and fecundity gene including conservation and development strategies for this remarkable sheep.
Received: January 26, 2010;
Accepted: March 28, 2010;
Published: May 29, 2010
Sheep are the very good economic converter of grass into meat, milk and wool.
In fact, there is no substitute for sheep as a class of livestock for utilizing
wastelands, stubbles of cultivated corps, tree topping, farm wastes or weeds
from the field. No domestic animals are capable of existing on such a variety
of food like weeds, grasses, shrubs, roots, cereals, leaves, barks (Sahana,
2001). Sheep utilize very sparse and low set vegetation for feed due to
its extremely close grazing nature for bifid upper lip and therefore never compete
with goat or cattle. With their small muzzles and split upper lips, they can
nibble tiny blades of vegetation, which also cannot be eaten by bigger animals
(Banerjee, 1989). In India sheep contribute greatly to
the agrarian economy, especially in the arid/semi-arid and mountainous areas
where crop and/or dairy farming are not economical. They play an important role
in the livelihood of a percentage of small, marginal farmers and landless laborers
engaged in sheep rearing. Moreover, throughout the world, when animal infertility
is a common and acute threat, we are having a sheep with higher fertility. A
number of rural based industries use wool and skin from sheep as raw material.
Sheep manure is an important source of soil fertility especially in Southern
The FAO global inventory of Livestock Breeds (FAO, 1987)
and World Watch List for Domestic Animal Diversity (DAD), (Loftus
and Scherf, 1993) estimated the total number of breeds of sheep was 863
in the world. Of these 101 are listed, as at risk and the status of many more
has not been adequately characterized. Mason (1980)
and Banerjee (1989) also listed over 800 breeds of sheep
in the world, whereas 59, breeds of indigenous sheep are identified so far in
India (Das, 2000). Most of our textbook refer that 42
descript sheep breeds are listed in India (Singh, 2000).
Many scientists defined the number of descript sheep breeds of India are 40
relating to region or utility (Acharya and Bhat, 1984;
Acharya, 2000). Majority of Indian sheep population
(75%) are nondescript (Singh, 2000).
Bengal Garole sheep has not been reported as a separate breed having distinguishable
breed characteristics. Garole is a native and local sheep of Bengal in extended
costal Sundarban area having distinct and separate phenotypic characters, productive
performances of their own is not thoroughly characterized and established as
Breed. This distinct but inadequately studied line of small sheep (locally named
as Garole) is the dominant domestic species isolated so far pointed out at this
extended coastal swampy Sundarban delta of West Bengal (Banerjee,
2008). This sheep is the latest sensations in the world of domestic species
by virtue of its prolificacy, lambing frequency, disease resistance and other
extraordinary merits rarely or not even observed in other sheep breeds of the
world. Historical evidence favours the assumption that the acclaimed Fecundity
gene (Booroola) in Australian Merino is derived from this Bengal line having
high prolific trait (Turner, 1980, 1982;
Piper and Bindon, 1996). Authentically not much is known
about the origin of the Garole sheep. However, based on survey work and local
farmer interrogation it is assumed that this domestic Garole sheep (Ovis
aries) might have originated from the wild urial type (O. vignei)
of Asia. The extremely hot, humid, saline climate with heavy rainfall and cyclone
prone riverine deltas of Sundarban made naturally occurred beneficial mutation
in fecundity gene of todays Bengal Garole, which is being well adapted for a
long time in its native tract. Annual average rainfall, maximum and minimum
temperature and relative humidity of this tract is 1622 mm, 36.5 and 12.0°C
and 87.5 and 79% (Year wise data book, 1997-2006, Government of India (Pan
et al., 2004). The native tract of this sheep is around 6210.867
sq. km extending coastal Sundarban area of West Bengal located between 21°32'
to 22°40' North latitude and 88°05' to 89°00' is longitude having
the boundary of river Hooghly on the West and the Bay of Bengal on the South.
The sheep Garole is very popular for its bi-annual lambing, multiple birth,
grazing on aquatic weeds and grass in knee-deep water and disease resistance
characters (Banerjee, 2008). They are small in size, produce
rough wool, good quality skin, manure and low fat mutton. Milk is having no
importance as the quantity is too less to feed its kids, although, it is very
much costly and popular locally for feeding and treatment of infant babies in
mouth ulceration. This small compact meat type animal predominantly white in
color, are owned by landless and small farmers which provide principal source
of income during agriculturally lean period and govern socio-economic status
of the sheep farmers of this region. The presence of the super-ovulatory gene
and other important character in these Sheep has seldom been seriously studied
in India (Bhattacharya, 1989).
Garole Sheep and its Farming
There is paucity of information on Garole sheep. Importance of high prolificacy
of this breed was seldom appreciated widely. But it had been reported by Turner
(1980, 1982), Piper and Bindon
(1996) that the high incidence of multiple birth in Merino was due to a
single gene (Booroola), which might have been migrated from the Bengal sheep
in late 18th Century. Mason (1980), Acharya
(1982), Bhattacharya (1989) and Kar
and Prasad (1992) pointed out distinct but inadequately studied unique type
smaller lines of local sheep (commonly known as Garole) which were geographically
restricted in costal Sundarban area of West Bengal. Mason
(1988, 1996) in his book A World Dictionary of Livestock
Breed Types and Varieties, mentioned that Garole, a dwarf prolific meat type
sheep of Bengal where males were horned and females were polled. He also noted
that the Garole could be compared with Bangladeshi. Actually, Hasnath
(1980) described similar type of sheep with adult body weight of 16.8 kg,
having the characteristics of high twinning rates and coarse wool production
in adjacent areas of Bangladesh. Both the sheep were not similar in characteristics
but could be comparable. According to survey results of Banerjee
and Banerjee (2000) and Pan et al. (2004) in
different locations of Sunderban area, it revealed that Garole was also called
as bhera and mera to male and female or horned and polled by local people. There
was no reference of this sheep as a breed but as variety by Mason
(1988, 1996), whereas, Acharya (1982)
and Acharya and Bhat (1984) referred Garole as little
knowing breed. The United States National Research Council listed this sheep
as microsheep based on measurements made on adult sheep. As per Board of Science
and Technology for International Development (BOSTID) small sized sheep were
discussed in chapter 3 of the book Microlivestock, but the breeds described
were about twice the size of the Garole. According to Ghalsasi
and Nimbkar (1993), Bose (1995, 1996),
Das (2000), Sahana et al.
(2001), Sahoo and Pan (2002), Pan
and Sahoo (2003) and Pan et al. (2004), the
sheep was very popular for its biannual lambing, multiple birth, grazing on
aquatic weeds and grass in knee-deep water. Nimbkar et
al. (2000), Bose (1995) and Ghalsasi
et al. (1994) also reported its disease resistance characters. Livestock
census report, Government of India in 1999, 1997 and 2004 illustrated that the
population of sheep in this tract was 2 million, which was very much static
from 1994 to 2004.
Ghalsasi and Nimbkar (1993) studied reproductive traits
viz. number of lambs born per ewe, age of first lambing with lambing interval
etc. and recorded impressive performance of Garole sheep. Bose
(1995, 1996), Singh and Bohra
(1996) and Sahoo and Pan (2002) mentioned the social
and economic impact of Garole sheep. These sheep are owned by landless and small
farmers and provide principal source of income during agriculturally lean period
and thereby govern socio-economic status of this region.
Phenotypic Characteristics of Garole Sheep
Phenotype characters such as ear length, tail length, horns, head profile,
wattles or beard, body size and conformation of Garole were reported by different
scientists. It has been observed that they are small in size, produce rough
wool and low fat mutton (Ghalsasi et al., 1994;
Banerjee and Banerjee, 2000; Singh
and Bohra, 1996; Sahana et al., 2001; Das,
2000). This small compact meat type animals predominantly black, white and
fawn or brown in coat color with black patch at lower portion of the body (Ghalsasi
et al., 1994; Nimbkar et al., 1998;
Bose et al., 1999, 2000;
Bose and Maitra, 1999; Sharma et
al., 1999). Bose et al. (1999), Sharma
et al. (1999), Das (2000), Banerjee
and Banerjee (2000) and Pan et al. (2004) illustrated
different ranges of ear length (long or pendulous or >6 cm, medium or erect
or 3-6 cm, rudimentary or <3 cm), tail length (>15, 5-15 or <5 cm)
horns (in male), head profile (concave, straight or convex), wattles or beard
(no wattles or beard), body size and conformation (weight of adult male 8-10
kg, adult female 10-14 kg, adult male and female chest girth 58-65 cm, adult
male and female height at wither 42-49 cm adult male and female body length
Litter Size in Sheep Including Garole
A number of reports on the litter size of Garole sheep are available from
different places. Ghalsasi and Nimbkar (1993) reported
the average liter size of Garole as 2.27 with 7.3% single, 65.45 twins 21.8%
triplet and 5.45% quadruplet, while Ghalsasi et al.
(1994) found average litter size of 2.23 with 9% single, 65% twin, 21% triplet
and 5% quadruplet. Sharma et al. (1999) noted
average litter size of Garole as 1.68 with 40% single, 53.33% twins, 5% triplet
and 1.67% quadruplet. However, Bose et al. (2000)
recorded litter size in Garole as 1.74 with percentage of single, twin, triplet
and quadruplet is 41.63, 43.35, 14.81 and 0.21, respectively. According to Pan
et al. (2004) average lambing frequency was within 1.63-1.94 and
with single 24% twin 66.4%, triplet 11.5% and quadruplet 0.2%. Singh
and Bohra (1996) published average litter size at first lambing in Garole
as 2 and in subsequent lambing it was 2-3 with single birth frequency of 25-30%,
twins 55-60%, triplet 15-20% and quadruplet 1-2%. According to Nimbkar
et al. (1998) average litter size was 2.3±0.9 with percentage
of single 35%, twins 57%, triplet 7% and quadruplet 1% in deccan plateau of
Maharashtra. In a recent survey in the native tract of Bengal Garole it was
reported that Garole had liter size of 1.855 with 23.9% single birth, 67.22%
twins, 8.31% triplet and 0.57% quadruplet was recorded (Banerjee,
2008). Fitch (1989) reported average lambing rate
of 2.4 in Garole and observed that the sheep could breed throughout the year.
Ghalsasi and Nimbkar (1993) reported average number
of lambs born per ewe in Garole was 2.27 (prolificacy-227%) in its native tract,
however, Ghalsasi et al. (1994) reported a lower
value of 2.23 (223%). In present study, we have noticed during evaluation of
phenotypic data, mean number of lambs born per ewe in Garole is 2.04 (prolificacy-204%)
in its native tract and 1.93 (prolificacy-193%) as an average of native and
out tract of Bengal (Banerjee et al., 2009a,
b). It may be due to indiscriminate or unplanned cross
breeding resulting dilution or adulteration and erosion of mutant FecB
genotype from its native tract. Although, these animals isolated geographically
in different Islands surrounded by rivers and sagars in its native tract, we
may lose this precise valuable outstanding genetic resources completely in near
Karyotype of Sheep Including Garole
From the chromosomal study of black karakul ewe, the diploid number of chromosome
was recognized as 2n = 54, 52 being autosomes and 2 being sex chromosomes (Shirinskii
et al., 1982). The autosomes were found to be metacentric (3 pairs)
and acrocentric (23 pairs), the X chrosomes being acrocentric. De
Oliveira Filho (1978) observed the diploid chromosome number of crossbred
Polworth rams to be 54 with 6 large metacentric and 46 acrocentric or telocentric
autosomes. Bunch and Foote (1976) observed that the
diploid chromosome number of Iranian sheep breeds was 54 with 3 pairs metacentric
and 23 pairs acrocentric autosomes. Babar et al.
(1991) and Mukhamedgaliev et al. (1974) reported
that sheep breeds viz., Lohi and other breeds of Kazakstan had 54 numbers
of chromosomes with 6 submetacentric and 46 acrocentric chromosomes where X
chromosome was the largest acrocentric or metacentric and the Y chromosome was
the smallest submetacentric. Similar report is available from McFee
et al. (1965). Rakshit et al. (1999)
found similar morphology in Sahabadi and Muzzarffarnagari sheep of India without
clearly configured Y chromosome. Akhuli (1999) and Banerjee
et al. (2008) studied the metaphase chromosome of Garole in its native
tract and Muzaffarnagri sheep, where it was observed that chromosome of these
breeds included 3 pairs submetacentric, 23 pairs acrocentric autosomes, acrocentric
X chromosome and smallest dot like Y chromosome.
Montgomery et al. (1994) reported that fecundity
gene was present in chromosome 6 of ovine species. However, there was no study
regarding genome length, chromosome length, centromere index or investigation
of chromosomal abnormality and its correlation of high fecundity of Garole sheep
of Bengal. Bahri and Cribiu (1989) studied on Tunisian
sheep and Chevelev (1986) studied on Soviet domestic
sheep, Rcheulishvili and Dzhokhadze (1985) studied the
Imeritian sheep, where all of them found no significant variation in genome
length between breeds, sex and between different locations among breeds of sheep.
Roy et al. (1991) pointed out that chromosome
of local indigenous sheep of Orissa was 54 in diploid stage including 3 pairs
submetacentric, 23 pairs acrocentric autosomes, acrocentric X chromosome and
elongated dot like Y chromosome. Bhatia and Shanker (1989)
reported the metaphase mitotic chromosomes in Nali sheep India which had karyotype
consisted of 3 pairs of metacentric and 23 pairs of acrocentric chromosomes
with largest acrocentric X chromosome and small biarmed metacentric Y chromosome.
Mulsant et al. (2001) reported that a single
nucleotide mutation in fecundity gene showed moderate to higher prolificacy
and lambing frequency in Booroola Merino. Ansari et al.
(1996, 1999) reported the variation of Idiogram
assay between breed and sex of sheep.
Genetic Speciality of Garole Sheep
The phenotype in Booroola merino is reported to be due to the mutant fecundity
gene, Bone Morphogenetic Protein Receptor IB (BMPR-IB) (Wilson
et al., 2001; Mulsant et al., 2001;
Montgomery et al., 1995a, b,
2001). They also observed that BMPR-IB receptor of ovarian
granulosa cell dimerized with BMPR-II and transmit signal through its natural
ligant BMP 4, BMP 7 and GDF 5 for progesterone secretion. However, if BMPR-IB
is mutant, it lost its responsiveness regarding progesterone secretion in ovarian
tissue. As a result FSH stimulated estrogen production would be enhanced at
oestrus (ovulatory peak) followed by FSH suppressed progesterone secretion would
be increased if there was pregnancy. They also opined that Booroola-Merino sheep
of Australia were characterized by high ovulation rate and litter size due to
mutation in FecB gene present in Chromosome No. 6. The Booroola strain
was developed through introgression of this FecB mutation from Indian
Garole to Australian Egelabra Merinos (Turner, 1982).
Davis et al. (2002) published evidence on origin
of this Booroola (FecB) mutation present in Booroola-Merino was from
Indian Garole sheep present in Costal Sundarbans area of West Bengal.
Fecundity Gene in Garole
Throughout the world, when infertility of sheep is a threat, historical
evidence and different molecular tests demonstrated the presence of naturally
occurred beneficial mutation in a major gene (FecB) in Indian Garole
(the sheep of Bengal) related to higher prolificacy and lambing frequency in
its native tract (Banerjee et al., 2009a). According
to Turner (1980, 1982 and 1983)
highly prolific Booroola Merinos can be traced back to an early Australian flock
known to include prolific Indian (Bengal) Garole sheep. Highly prolific Garole
sheep of West Bengal, India have many of the fleece and body characteristics
reported for the early Bengal sheep in Australia (Piper and
Bindon, 1996) and the two names possibly refer to the same sheep or very
closely related breeds. Recent molecular tests demonstrated by different scientists
(Davis et al., 2002; Montgomery
et al., 2001; Wilson et al., 2001)
established possible link regarding transmission of this beneficial mutation
present in Bengal Garole to Australian Booroola Merino with high litter size
and lambing frequency. Piper and Bindon (1996) defined
the acclaimed genesis of Fecundity gene, FecB (Booroola) in Australian
Merino as from the Bengal line having high prolific trait.
A preliminary study determined the segregation pattern of marker DNA fragment
associated to the fecundity gene in Garole. National Bureau of Animal Genetic
Resources (NBAGR), Karnal, India recorded a summary of micro-satellites exhibiting
amplification in Garole sheep in their Annual Report in 1998-1999. Sodhi
et al. (2003) studied the genetic characterization of Garole sheep
using microsatellite markers and observed high level of genetic heterogeneity
that was reflected in Garole sheep. Davis et al.
(1982) and Piper and Bindon (1982a, b)
observed that the Booroola fecundity gene (FecB) increased the ovulation
rate and litter size in sheep and was inherited as a single autosomal locus.
Montgomery et al. (1993, 1994)
reported that FecB was located on sheep chromosome 6 between SPP-1 and
EGF genes at chromosome 6q23-31 region which was syntenic group to
human chromosome 4q21-25 region (Lanneluc et
al., 1994, 1996). This FecB contained
the BMPR-1B gene, considered as positional candidate to affect steroid synthesis
of ovarian granulosa cells and oocytes (Hogan, 1996;
Massague, 1998). Shimasaki et
al.(1999) observed that BMPR-1B encoded a member of the transforming
growth factor-β (TGF-β) receptor superfamily responsible for inhibitory
effect on steroidogenesis of GDF-5 and BMP-4, natural ligands of BMPR-1B. Wilson
et al. (2001) published novel findings regarding Booroola genotypes
which had a nonconservative substitution (Q249R) in the BMPR-1B coding sequence.
He found partial inactivation of BMPR-1B, leading to an advanced differentiation
of granulosa cells and an advanced maturation of ovulatory follicles associated
fully with the hyperprolificacy phenotype in Booroola ewes. Wilson
et al. (2001) and Mulsant et al. (2001)
revealed a point mutation in a major gene, fecundity booroola (FecB)
in chromosome number 6 results higher prolificacy in Garole but not in other
breeds of sheep or its wild variety. The nucleotide sequence obtained in mutant
FecBB allele was identical to the wild type allele, except
for A→G (adenine to guanine) transition position 746, substituting the
amino acid sequence, glutamine present in the wild type sequences as well as
in human and mouse sequences to arginine (Mulsant et
According to the recent findings of Davis et al.
(2002), BMPR-1B mutation was found in Indian Garole, Booroola and
Javanese sheep. Frequency of homozygosity of mutant allele in Garole of India
was higher than Booroola and Javanese sheep linked with higher prolificacy.
Inheritance patterns suggested possible migration of major genes affecting prolificacy
from Indian Garole to Australian Booroola-Merinos and in case of Javanese sheep
it was directly from Garole or via Booroola-Merinos from Garole.
Fecundity Gene, its Mutation and Productivity
Pardeshi et al. (2005) studied to assess
the FecB mutation in four Indian sheep breeds, viz., Garole, Deccani,
Bannur and Madras Red and its introgression with relation to productivity and
reported that only Garole possessed double copy FecB mutation with higher
fecundity (Banerjee et al., 2009a) but Deccani,
Bannur and Madras Red possessed one copy with medium fecundity in F1 after
crossing with Garole. Mulsant et al. (2001) reported
mutation in bone morphogenetic protein receptor-IB (BMPR1B) was associated
with increased ovulation rate in Booroola Merino ewes. Yi
et al. (2001) observed the type I BMP receptor BMPRIB was
essential for female reproductive function on the actions of several hormones,
signaling in early stages of folliculogenesis. Juengel and
McNatty (2005) reported that proteins of the transforming growth factor
beta (TGF-β) superfamily, growth differentiation factor 9 (GDF9), bone
morphogenetic protein 15 (BMP15) and BMP6 regulate intra-ovarian follicular
development in female. Juengel et al. (2006)
studied on bone morphogenetic proteins 2, 4, 6 and 7 and observed that these
proteins would have an important intra-ovarian role in regulating follicular
development in sheep and rat.
Montgomery et al. (2001) reviewed genes controlling
ovulation rate in sheep. Galloway et al. (2000)
observed mutations in an oocyte derived growth factor gene (BMP 15) caused increased
ovulation rate and infertility in a dosage-sensitive manner in many breeds of
sheep. Walling et al. (2000a, b)
made characterization and mapping of the Booroola (Fec B) gene using
regression analysis in sheep and consequences of carrying the booroola fecundity
(Fec B) gene on live weight. Piper and Bindon (1982a,
b) presented first evidence for segregation of a locas
with a major effect on litter size in the Booroola strain of Merino sheep. Subsequently
Davis et al. (1982) and Davis
(1985) showed in New Zealand Booroola flocks to result from its additive
effect on ovulation rate using imported genetic material. Thereafter many breeds
of sheep with high fecundity or prolificacy had been evaluated by different
scientists like Belle-Ile sheep of France by Mahler and
Lechere (1998), Cambridge of Australia by Owen et
al. (1990), Thoka, Icelandic sheep by Jonmundsson
and Adalsteinsson (1985), Javanese sheep of Indonesia by Bradford
et al. (1986), Lacaune sheep of France by Bodin
et al. (1998), Beclare sheep by Hanrahan (1991),
Olkuska sheep by Radomska et al. (1988) having
autosomal inheritance. Davis et al. (2002) reported
the presence of FecB mutation was in the Garole and Javanese sheep only
but not in Cambridge, Thoka, Lacaune, Belclare and Olkuska sheep. Davis
et al. (1995) discovered inverdale gene, which is X linked inheritance
in Romney sheep of New Zealand with high prolificacy. Davis
et al. (2001) further evidenced that an imprinted gene on the X chromosome
increases ovulation rate in woodlands sheep of New Zealand.
Reproductive Function of BMP Gene
Otsuka et al. (2001) provided the first insight
into the biological function of BMP-6 in the ovary and demonstrated its unique
mechanism of regulating FSH action resulting marked decrease in Follicle-Stimulating
Hormone (FSH)-induced progesterone production but not estradiol through selective
modulation of FSH action in steroidogenesis. According to Shimasaki
et al. (2004) role of the Bone Morphogenetic Protein (BMP) family
of growth factors in the reproductive system using molecular, cellular and genetic
approaches, had led to significant breakthroughs in our understanding of mammalian
reproduction and fertility and reviewed thoroughly the evidence underpinning
the importance of the BMP system in mammalian reproduction. Campbell
et al. (2006) worked on enhanced response of granulosa and theca
cells in sheep having carriers of the mutant FecB. In vitro study
on gonadotropins and bone morphogenic protein 2, 4 and 6 made evidence to support
the hypothesis that, FecB mutation increases the BMP response of somatic
cells when stimulated to differentiate by gonadotropins. Faure
et al. (2005) observed bone morphogenetic protein (BMP-4) inhibits
follicle-stimulating hormone secretion in ewe pituitary. It revealed the presence
of a functional BMP system which operates in the sheep pituitary at least, in
vitro to decrease FSH release and to modulate the effect of activin.
Pierre et al. (2004) studied on molecular basis
of bone morphogenetic protein 4 inhibitory actions on progesterone synthesis
by ovine granulosa cells, which was a new implication in understanding the role
of BMP family members in the control of ovarian folliculogenesis. Hanrahan
et al. (2004) reported first lime that a mutation in the gene for
GDF9 causes increased ovulation rate and infertility in a manner similar to
inactivating mutations in BMP15 and showed that GDF9 is essential for normal
folliculogenesis in Cambridge and Belclare sheep. Furthermore, it is shown,
for the first time in any species, that individual with mutations in both GDF9
and BMP15 have a greater ovulation rate than sheep with either of the mutations
separately. According to Nilsson and Skinner (2003),
Bone Morphogenetic Protein 4 acted as an ovarian follicle survival factor and
promoted primordial follicle development in rat ovaries.
Xia et al. (2003) studied on the concentrations
of progesterone, follistatin and Follicle-Stimulating Hormone (FSH) in peripheral
plasma across the oestrous cycle and pregnancy in merino ewes that are homozygous
or noncarriers of the booroola gene. The Booroola phenotype was due to a point
mutation in the BMP1B. Progesterone concentrations began to rise earlier and
were higher in the Booroola ewes than in the noncarriers in luteal phase but
not during the follicular phase of the cycle. Follistatin concentrations remained
unchanged across the oestrous cycle in both groups of ewes, with no differences
between genotypes. FSH concentrations were higher in Booroola ewes than in noncarrier
ewes on most days of the oestrous cycle, with a significantly higher and broader
peak of FSH around the time of oestrus. Progesterone concentrations were significantly
higher in early and mid gestation in Booroola ewes but were lower toward the
end of gestation than those in noncarriers. These results suggested that progesterone
and FSH not follistatin concentration was being regulated by the FecB
gene during the estrous cycle and pregnancy. Pepin et
al. (2003) published expression profiles and chromosomal localization
of genes within BMP families and oocyte derived factors controlling meiosis
and follicular development in the cyclic Ile-de-France sheep ova useful to identify
potential candidate genes that might underlie these effects.
Meat, Skin and Wool Productivity of Sheep Including Garole
A wide variation in dressing percentage of Garole sheep has been reported
by various authors. Bose (1995), Bose
and Maitra (1999) recorded dressing% of Garole sheep as 48.26%, whereas,
Banerjee and Banerjee (2000) and Das
(2000) reported dressing% in Garole sheep as 52 and 66.54%, respectively.
Singh (1998) observed dressing percentage of 53% in other
Indian sheep breeds. Prasad (1997) noted variation in
dressing percentage in male and female to the tune of 45-53% and 40-45%, respectively.
Pal et al. (1997) reported dressing percentage
of 44.61% and 48.49% in Muzaffarnagari lambs maintained under semi-intensive
and intensive systems, respectively. According to Pan and
Sahoo (2003) and Pan et al. (2004) carcass
parameters like slaughter age of Garole sheep were 8-12 months in male and above
24 months in female; whereas slaughter weights were on an average 10-12 and
13 kg for male and female, respectively. Carcass weight of male and female animals
were, however, 6.61-8.66 and 6.59 kg. Blazquez et al.
(2001) observed significant differences in carcass and meat quality of sheep
belonging to different body weight groups of 5 and 25 kg.
Crosby (2000) discussed on the need to improve marketing
of lamb meat, mutton and mutton products through quality assurance, sheep traceability,
tagging and the scrapie monitoring/testing programme. Ruiz
de la Torre et al. (2001) recorded variation in pH, color, few kinase
and dehydrogenase enzymes activity of sheep carcass as stress responses during
transportation. In general, meat is composed of water (75%), fat (3%), protein
(19%), non protein nitrogenous substances (1.5%), minerals (1%) and a small
portion of carbohydrate (Lawrie and Ledward, 2006). Lipid
is the most variable of these components, but is closely and inversely related
to the water content. Researchers reported sheep meat standards like moisture
73.0%±0.1, protein 18.9%±0.05, fat 6.0%±0.2, ash 1.5%±0.2,
carbohydrate and vitamin etc 0.6%±0.002. They also noted that, moisture%
is inversely related with fat%. Banerjee et al. (2009b)
reported that dressing percentage of 55.87 in Garole sheep. The meat had pH,
water holding capacity and refrigeration loss of 5.96, 43.33 and 0.86%, respectively.
They further reported moisture, protein, fat, ash and carbohydrate content as
76.02, 18.20, 3.53, 1.65 and 0.60%, respectively.
Shackelford et al. (2005) made research regarding
effects of breed on lamb meat quality. The experiment was conducted to compare
the meat quality and carcass composition of a diverse sampling of sheep breeds.
No single breed excelled to a great degree in carcass composition. Therefore,
they are to improve lamb quality exploring breed effects using the most appropriate
breeds in crossbreeding programs that produce market lambs. According to Watt
and Merrill (1963) lowered pH and water holding never damage appearance
(dark) and flavour as well as prevents bacterial growth and spoilage. Therefore,
due to these qualities along with lowered refrigeration loss helps in long-term
meat preservation also observed by Callow in 1948.
Zinc, cupper, iron, manganese, sodium, potassium and chloride are the major
minerals in meat, which influence nutritive value of mutton (Rice,
1971). Meat is a good source of different minerals mainly dietary iron and
phosphorus except calcium (Landmann, 1960). Magnesium,
copper and zinc have been reported as highly essential in meat based baby foods
(Vazir, 2003; Medappa, 2003;
Daglioglu et al. (2001) carried out a comparative
examination of the skin, leather properties and the histological structures
of skin of different sheep genotypes. The thickness of total skin, epidermis,
dermis, stratum superficiales and stratum profundum were measured. Density and
the thickness of collagen and elastic fibres in dermis sublayer and density
of wool follicles were established. The results were compared among three genotypes
of sheep. Histometrical properties of Kivircik and crossbred lambskins were
similar to each other but skin properties Merinos were different from other
two genotypes. Prasad (1996,1997)
examined all skin parameters and observed that sheep skin were valuable for
leather industry producing leather coats, jackets, shoes, gloves, robes, rugs,
slippers etc. According to Pan and Sahoo (2003) and Pan
et al.(2004) skin parameters like skin length, skin width, skin area,
skin weight and skin weight percentage of skin of adult Garole sheep was around
65.3-84.1, 59.7-63.2 cm, 4048.3-5474.1 sq. cm, 1.2-2.3 kg and 10.5-12.0%, respectively.
Banerjee et al. (2009b) also reported almost
Horton and Rodriguez (1997) compared between hair
(St. Croix) and wool (Targhee and Dorset) of lambs and the effect of heat stress
on food and water intake, digestive function and nitrogen balance. They concluded
that hair sheep were more heat-tolerant than wool sheep, as they consumed more
feed, gained more body weight and improved digestibility when exposed to elevated
temperatures. It is observed the significant effect of cortisol acetate on wool
quality in sheep selected for divergent staple strength. Smuts
et al. (2001) evaluated the role of sheep breed and mohair style
and character in the OFDA curvature vs. staple crimp/wave frequency relationship.
They summarized that the OFDA curvature can be used as a measure of wool staple
crimp and mohair wave frequency without the need to take either sheep breed
or mohair style and character into consideration. Wool Grading and Marketing
Rules mentioned to issue Conditioning Certificate which denotes clearance from
quality control through different gradation testing procedures. Rodney in 1993
demonstrated different methods like American system, English or Spinning count
system and the Micron system to evaluate certain qualities such as fineness,
length, color and appearance that determine the end use and value of wool. He
also discussed, fineness, the fiber diameter and its distribution, as the most
important quality factors for grading. Fineness largely determines whether the
wool is used in a suit, sweater and blanket or in a pair of socks. Singh
(1997) elaborately discussed regarding all aspects of wool growth, structure,
production, properties, grading and processing. Wool Research Association, Thane
in their annual report of 2001-2002 defined different methods for quality testing
and grading of wool for production of good quality wool and followed by upgradation
of Indian wool Industry. Benavides and Maher (2003)
worked on wool color and skin traits to assess phenotypic and genetic correlations
between wool color and skin traits. They found that skin traits had high genetic
correlation with clean wool and color of wool which might be useful for indirect
selection of these traits.
Bose (1996) and Bose et al.
(1999) studied on wool characters of Garole sheep. They showed that wool
of Garole was extremely coarse, hairy and not very dense. Bose
and Maitra (1999) defined annual average greasy fleece yield from each Garole
sheep was 152 g. According to Ghalsasi and Nimbkar (1993)
Garole wool was quite coarse. Sharma et al. (1999)
observed average annual adult wool yield from each Garole sheep procured from
Sundarban area was 179 g which was for rough carpet use. Singh
and Bohra (1996) studied on wool parameters of Garole sheep and reported
that average wool yield was 150 g per shearing from each sheep, which was of
rough carpet type. Prasad (1996, 1997)
also reported average annual production of wool per sheep was around 300 g.
They studied fibre parameters like average fibre diameter, medullation, staple
length and crimp/cm of Garole sheep which were reported to be 67.82 μ,
75.17%, 5.09 cm and 2.08, respectively. On the other hand Pan
and Sahoo (2003) and Pan et al. (2004) recorded
fibre diameter, medullation and fibre length as 53.02 μ, 78.7% and 4.99
cm, respectively in Garole sheep. They observed that shearing was not at all
common practice, although each Garole was capable to yield approximately 400
g greasy fleece annually.
Disease Resistance in Sheep Including Garole
Internal parasitism and a few bacterial or viral diseases create a great
threat to sheep industry. Indian sheep in general have low prolificacy and high
worm infestation, which greatly affect productivity around most agro climatic
regions of the country. The main impact of these infections is decreased appetite
and disturbances on energy, protein and mineral metabolisms leading to reduced
productivity. Further, some blood protozoa or blood sucking parasites causes
anaemia and sometimes leads to death in severe infection. Apart from these,
some bacterial diseases such as foot rot or infectious pododermatitis, Gid (Multiceps
multiceps) and viral diseases as PPR, FMD, sheep pox and malignant ovine
spongiform encephalopathy damage the sheep husbandry. Different anthelmentics,
antibiotics and vaccines may be advocated against these infections. However,
recently anthelmentic or drug resistance is posing a problem which necessitate
the development of sustainable Integrated Pest Management (IPM) principles for
worm control and/or genetic resistance of host against some bacteria or virus.
Selection of host for individual genetic resistance towards parasite, bacteria
or virus followed by their crossing to increase their frequency in the population
is highly expected for the future generations. Gradually disease resistant strains
against selective diseases are developed e.g., in East African Red Maasai, Florida
Native and St. Croix which are relatively worm resistant sheep breeds (Garran
and White, 1985).
Interestingly Indian Garole have naturally developed resistance against natural
and induced parasitic infections, foot rot, FMD, reproductive disorders etc.
Garole sheep are considerably more resistant to dreaded round worm Haemonchus
contortus as well as to the tropical liver fluke (Nimbkar,
2002). During authors survey hardly even single foot rot or FMD infection
was found in its native tract (Banerjee, 2008). Garole
sheep was identified mainly due to its high prolificacy but it was also hoped
that it might have some useful genes for resistance to internal parasites, liver
flukes and different bacterial or viral diseases. There is evidence that major
autosomal genes affect host resistance to nematode parasites in Coopworth sheep
that strongly support Garole phenomenon (McEwan and Kerr,
1998). Background of disease resistant feature in Garole is not well known
clearly, however, it might be due to differential γ-globulin expression
than other breeds because of its power of adoption against natural stressful
extreme costal climate in its native tract as γ-globulin is one of the
most defined immunomodulator, concentration of which determines individual resistance
to diseases. Significant gamma immunoglobulin expression assay was done to understand
the outstanding disease resistant characters of Garole (Banerjee,
Pan et al. (2004) recorded no trematode infection
in Garole sheep and incidence of gastrointestinal tract infection was around
54.6% followed by abortion, repeat breeding, placenta retention and post-gestational
mortality, was 7.82, 9.35, 2.62 and 14.08%, respectively and miscellaneous infection
was also seen around 20.6%. Kooyman et al. (1997)
found differential elevated immunoglobulin (IgE) level in sheep at normal infection
with Haemonchus contortus resulted in significant increased level in
serum as measured by sandwich ELISA and Western blots. Engwerda
et al. (1992) reported resistance of one breed greatly varied on
source of immunoglobulin, the amino acid sequence of variable or constant region.
White et al. (2001) exhibited significantly different
expression in sheep gamma/immunoglobulin assay, challenged with gastrointestinal
nematode Haemonchus contortus by reverse transcriptase-polymerase chain
reaction (RT-PCR) from Abomasal Lymph Node (ALN) B cells due to gamma/immunoglobulin
(Ig) heavy-chain and lambda light-chain variable region nucleotide coding sequence
present in sheep genome. Murray and Smith (1994) observed
that level of host immunoglobulin greatly varies due to ingestion of it by Haemonchus
contortus, Ostertagia ostertagi, O.circumcincta [Teladorsagia
circumcincta] and Dictyocaulus viviparus, after staining of sections
of the worms with fluorescent anti-sheep immunoglobulin technique even by the
non-blood-feeding species, therefore, might be susceptible to vaccination by
the gut antigen approach. Hailat and Lafi (1998) identified
a deficiency in the Slow Moving Immunoglobulin in Awassi Sheep.
Seaton et al. (1992) detected different specific
serum antibody responses of sheep in L. cuprina infection by ELISA and
immunoblotting which were due to breed or individual variation in percent concentration
of immunoglobulin mainly IgG and IgM. Diez-Tascon (2005)
performed microarray analysis of selection lines from outbreed populations to
identify genes involved with nematode parasite resistance in sheep. Miresan
(2003) evaluated significant breed differences of main blood indices including
gamma globulin using electrophoresis technique in Tsigai fattening sheep, Merino
of Cluj and Corriedale breeds. Nimbkar et al. (2000)
performed an analysis regarding comparison of the growth performance and worm
resistance of lambs produced by diallel crossing of three Indian sheep breeds
like Deccani (D), Bannur (B) and Garole (G) and he proved that lambs sired by
G and B rams were more resistant to naturally acquired worm infections and to
artificial challenge with Haemonchus contortus than those sired by D
rams. However, lambs sired by D and B rams had higher birthweights and growth
to 6 months than those sired by G rams.
Zhang et al. (1998) observed genetic enhancement
of resistance to gastrointestinal worm infection predominantly Trichostrongylus
sp. when selection was done in genotypes used for meat type sheep production
in Australia. Waelchli et al. (1994) studied
on immunoglobulin concentrations in colostrum and serum of lambs of dairy sheep
breeds, which revealed lower colostral immunoglobulin concentrations, have no
negative impact on the serum immunoglobulin concentrations, provided that good
management practices are followed. McEwan and Kerr (1998)
evidenced that major autosomal genes affect host resistance to nematode parasites
in Coopworth sheep. Woolaston and Gray (1991) recommended
for improving genetic resistance of sheep diseases. They discussed the h2 of
faecal egg count, fleece rot and foot rot, their genetic correlations with other
traits and the mechanisms of resistance to these diseases focus a great impact
on disease resistant traits present in specific sheep breeds might be beneficial
for global ovine industry.
Conservation and Development Efforts for Garole
Nimbkar et al. (1998) established prolific
Garole sheep from Bengal in the semi-arid deccan plateau of Maharashtra through
selection and breeding. Its crossing with other local breeds by Nimbkar Agricultural
Research Institute (NARI), Phaltan, Maharashtra made it one of the most economic
and feasible animal husbandry programme of this state. Outstanding reproductive
performance of Garole had also been reported by Bose and
Maitra (1999) and suggested the scientific breeding of this local sheep
for improvement of economic conditions of the farmers. Singh
(2000) narrated that significant opportunity for active conservation of
sheep genetic resources remain. According to Fahmy (1996)
and Fahmy and Davis (1996) major genes for prolificacy
and body composition exist in this sheep. Because of these outstanding merits
scientists from other countries had been attracted several times to genetically
evaluate this particular breed.
The presence of the superovulatory gene and other important characters in these
sheep had seldom been seriously studied in India, which is highly necessary
to conserve and explore possible development of Garole. Das
(2000) demonstrated that need of in situ conservation of Garole sheep
was urgent in Bengal. He also stated that in the Xth Plan document of Planning
commission of Government of India a major thrush was given on it. Dasgupta
and Das (2005) strongly recommended in-situ conservation and development
of Garole sheep through strategic breeding policy in West Bengal. It is demonstrated
that Garole sheep had suffered enough degredation leading to diluted genetic
quality. He also stated that population size of true to the breed was reducing
fast, needed to be planned for conservation. In addition, he indicated that
the best way to conserve the resources was within their native environment (in
situ) with the direct involvement of stake holders and farmers. Pan
et al. (2004) reported that Garole sheep was facing a constant threat
from gradual shrinkage of grazing land and other feed resources. Therefore in
situ conservation of the genetic material with available feed resources
was the crying need of the time. Ahlawat et al. (2002)
emphasized that there was a strong need for genetic improvement programme in
Garole sheep at the farmers flock in order to make sheep rearing more profitable.
Due to static trend in population and negative trend in litter size, there may be immediate threat in sheep vis-à-vis Garole sheep of West Benga. In the same way, indiscriminate cross breeding during last few years has endangered a few important indigenous breeds of India (Jammu and Kashmir). Therefore, conservation programme in terms of in situ or ex situ may be of immediate need along with strong need for genetic improvement programme of Garole sheep at the farmers flock in order to make sheep rearing more profitable. Considering the importance of Garole sheep of Bengal, tenth plan document of planning commission, Govt. of India, mentioned it at risk and proposed for specific project for its conservation and development. For growing realization of the improvement of indigenous genetic resources because of their adoption to specific agro-ecological condition and for conservation of biodiversity, it is not only the production but the efficiency of production in relation to physical environment, feed resources availability, management practices and disease factors which ought to be considered in deciding the future plans and strategies. In order to give holistic approach to productivity performance of a group of animals, their performance should be tested in native system of production to evaluate their relative efficiency as well as cost benefit ratios.
There is no definite breeding strategy of sheep in West Bengal. However a state level symposium cum round table on Breeding policy for conservation of small ruminants of West Bengal organized by West Bengal University of Animal and Fishery Sciences, Kolkata in collaboration with Department of Animal Husbandry, Dairying and Fisheries, Government of India and Animal Resources Development Department, Government of West Bengal on 02.09.2005 recommended selective breeding for improvement of Garole sheep. It was also recommended to follow open nucleus breeding for the production of improved rams for fecundity and lambing frequency parameters. It was also decided to take action regarding ram mother farm production and exchange of rams to the farmers may be carried out at the earliest. Simultaneously, development of marketing facilities for skin, meat and meat products is to be done through promotion of self help groups and cooperative marketing structure. The West Bengal Government has of late, shown keen interest in this breed and desired to conserve and explore possible development of the breed by adopting a definite breeding strategy. It is expected to augment the economy of poor farmers maintaining these Sheep in the coastal region of West Bengal. This great gift of the nature must be preserved and propagated through scientific breeding and management in its native tract and all possible measures must be undertaken to fulfill this goal.
1: Acharya, R.M., 1982. Sheep and Goat Breeds of India. Food and Agricultural Organization, United Nations, Rome, Italy
2: Acharya, R.M., 2000. Management and conservation of livestock genetic resources- impact analysis. Proceedings of the National Workshop on Conservation and Management of Genetic Resources of Livestock, (CMGRL'00), National Academy of Agricultural Sciences, New Delhi, GOI, GBPUA and T, Pantnagar, India, pp: 9-23
3: Acharya, R.M. and P.N. Bhat, 1984. Livestock and Poultry Genetic Resources in India. IVRI Research Bulletin No. 1. IVRI Publication, Izatnagar, Bareilly, UP, pp: 76
4: Ahlawat, S.P.S., M.S. Tantia and G. Sahana, 2002. Conservation and development of garole sheep in Sundarban areas of Eastern region. Proceedings of the National Symposium on Prospect of Animal Resources in Eastern and North Eastern Region of India. IVRI (ERS), (NSPARENERI'02), Belgachia, Kolkata, pp: 36-39
5: Akhuli, S., 1999. Cytogenetic study on metaphase chromosome of garole and muzaffarnagri sheep. M.Sc. Thesis, Department of Animal Genetics and Breeding, West Bengal University of Animal and Fishery Sciences, Belgachia, Kolkata, West Bengal.
6: Ansari, H.A., A.A. Bosma, T.E. Broad, T.D. Bunch and S.E. Long et al., 1996. Resolving ambiguities in the karyotype of domestic sheep (Ovis aries). II. G-, Q- and R-banded idiograms and chromosome-specific molecular markers. Chromosoma, 105: 62-67.
7: Ansari, H.A., A.A. Bosma, T.E. Broad, T.D. Bunch and S.E. Long et al., 1999. Standard G, Q and R-banded ideograms of the domestic sheep (Ovis aries): Homology with cattle (Bos taurus). Report of the committee for the standardization of the sheep karyotype. Cytogenet Cell Genet., 85: 317-324.
8: Babar, M.E., Z. Ahmad and S. Ali, 1991. Studied on the karyotype of Lohi sheep. Pak. Vet. J., 11: 57-61.
Direct Link |
9: Bahri, I. and E.P. Cribiu, 1989. The chromosomes of two types of Tusian sheep. In African small ruminant research and development. Proceedings of the a Conference, Jan. 18-25, Bamenda, Cameroon, pp: 39-50
10: Banerjee, G.C., 1989. A Text Book of Animal Husbandry. 6th Edn., Oxford and IBH Publishing Co. Pvt. Ltd., New Delhi
11: Banerjee, R., 2008. Conservation and in situ development of a prolific indigenous sheep in the Sundarban and Sagar Island. Ph.D. Thesis, University of Calcutta, Kolkata, West Bengal, India.
12: Banerjee, R., B. Manna and A. Roy, 2008. Karyotype study in three Indian ovine populations, Garole, Shahabadi and Muzaffarnagari and it`s correlation with reproductive efficiency and prolificacy. Proc. Zool. Soc., 61: 9-18.
13: Banerjee, R., A. Gupta and K. Ray, 2009. Assessment of the FecB mutation in three Indian sheep breeds including Garole in its native tract and its effect on prolificacy. ACIAR, 133: 229-230.
14: Banerjee, R., P.K. Mandal, S. Bose, M. Banerjee and B. Manna, 2009. Quality evaluation of meat, skin and wool from garole sheep-a promising breed from India. Asian J. Anim. Sci., 3: 39-46.
CrossRef | Direct Link |
15: Benavides, M.V. and P. Maher, 2003. Genetic parameters of wool colour and skin traits in Corriedale sheep. Genet. Mol. Biol., 26: 267-274.
16: Bhatia, S. and V. Shankar, 1989. Chromosomes of nali sheep. Indian J. Anim. Sc., 59: 297-299.
17: Bhattacharya, N.K., 1989. An Overview-Goats. In: Animal Productivity, Bhat, P.N., K.K.G. Menon and H.C. Srivastava (Eds.). Oxford and IBH Publishing Co. Pvt. Ltd., Calcutta, pp: 465
18: Blazquez, B., E. Miguel, E. Onega, F. Ruiz-de-Huidobro and de-Huidobro-F-Ruiz, 2001. Development of carcass and meat quality in sheep between body weight of 5 and 25 kg. Proc. Int. Symp. IX Jornadas Sobre Prod. Anim. Zaragoza, Spain, ITEA, 22: 643-645.
19: Bodin, L., J.M. Elsen, J.P. Poivey, S.M. Cristobal-Gaudy, J.P. Belloc and F. Eychenne, 1998. Hyperprolificacy in the french- lacaune sheep breed. Proc. World Cong. Genet. Applied Livest. Prod., 27: 11-14.
20: Bose, S., 1995. Bengal breed of sheep in the Sundarbans. Asian Livest., 20: 16-17.
21: Bose, S., 1996. Studies on the productive and reproductive performance of sheep in saline and semi-saline belt of West Bengal. Ph.D. Thesis, West Bengal University of Animal and Fishery Sciences.
22: Bose, S. and D.N. Maitra, 1999. Prospects of bengal sheep (garole): A hidden wealth in West Bengal. Indian J. Anim. Prod. Mamt., 15: 17-19.
23: Bose, S., R. Duttagupta and D.N. Maitra, 1999. Phenotypic characteristics and management practices of Bengal sheep. Indian J. Anim. Prod. Mamt., 15: 18-22.
24: Bose, S., R. Duttagupta and D.N. Maitra, 2000. Reproductive per formance of Bengal sheep in Sundarbans. Indian J. Anim. Prod. Mamt., 15: 157-160.
25: Bradford, G.E., J.F. Quirke, P. Sitorius, I. Inounu and B. Tiesnamurti et al., 1986. Reproduction in Javanese sheep: Evidence for a gene with large effect on ovulation rate and litter size. J. Anim. Sci., 63: 418-431.
26: Bunch, T.D. and W.C. Foote, 1976. Chromosomes, haemoglobins and transferring of Iranian domestic sheep. J. Heredity., 67: 167-170.
27: Campbell, B.K., C.J.H. Souza, A.J. Skinner, R. Webb and D.T. Baird, 2006. Enhanced response of granulosa and theca cells from sheep carriers of the FecB mutation in vitro to gonadotropins and bone morphogenic protein 2, 4 and 6. Endocrinology, 147: 1608-1620.
28: Chevelev, S.F., 1986. Chromosomes of domestic cheep. Veterinariya, 1: 27-29.
29: Crosby, F., 2000. Traceability and quality assurance. Irish-Grassland Anim. Prod. Assoc. J., 34: 132-134.
30: Daglioglu, S., A. Armutak, M. Ozcan, S. Boler and H. Akin, 2001. Comparative examination of the skin structures and leather properties of different genotype sheep which are farmed bandirma research institute. I. The comparative quantitative examination of the histological structures of skin. Veteriner-Fakultesi-Dergisi-Istanbul, 27: 513-534.
31: Das, D., 2000. Phenotypic, genotypic performance of garole sheep. Ph.D. Thesis, West Bengal University of Animal and Fishery Sciences, Kolkata.
32: Dasgupta, S.K. and N. Das, 2005. Plennary session recommendations. Proceedings of the State Level Symposium and Round Table on Breeding Policy for Conservation of Small Ruminants of West Bengal, (SLSRTBPCSRWB`05), Belgachia, Kolkata, India, pp: 36-39
33: Davis, G.H., 1985. Use of imported genetic material to increase prolificacy in sheep. Proceedings of the 15th Seminar of the Sheep and Beef Cattle Society of the New Zealand Veterinary Association, Ascot Park, Invercargill, May 23-24, Department of Veterinary Clinical Sciences, Massey University, Palmerston North, New Zealand, pp: 45-54
34: Davis, G.H., K.G. Dodds, R. Wheeler and N.P. Jay, 2001. Evidence that an imprinted gene on the X chromosome increases ovulation rate in sheep. Biol. Reproduc., 64: 216-221.
Direct Link |
35: Davis, G.H., J.C. McEwan, P.F. Fennessy and K.G. Dodds, 1995. Discovery of the Inverdale gene (FecX). Proc. N. Z. Soc. Anim. Prod., 55: 289-290.
Direct Link |
36: Davis, G.H., G.W. Montgomery, A.J. Allison, R.W. Kelly and A.R. Bray, 1982. Segregation of a major gene influencing fecundity in progeny of booroola sheep. N. Z. J. Agric. Res., 25: 525-529.
CrossRef | Direct Link |
37: Davis, G.H., S.M. Galloway, I.K. Ross, S.M. Gregan and J. Ward et al., 2002. DNA tests in prolific sheep from eight countries provide new evidence on origin of the Booroola (FecB) mutation. Biol. Reprod., 66: 1869-1874.
CrossRef | PubMed | Direct Link |
38: Diez-Tascon, C., 2005. Microarray analysis of selection lines from outbred populations to identify genes involved with nematode parasite resistance in sheep. Physiol. Genomics, 21: 59-69.
CrossRef | Direct Link |
39: Engwerda, C.R., R.A. Sandeman, S.J. Stuart and R. M. Sandeman, 1992. Isolation and sequence of sheep immunoglobulin E heavy-chain complementary DNA. Vet. Immunol. Immunopath., 34: 115-126.
40: Fahmy, M.H., 1996. Prolific Sheep. CAB International, Wallingford, Oxon, UK., Pages: 560
41: Fahmy, M.H. and G.H. Davis, 1996. Breeds with Newly Discovered Genes for Prolificacy. In: Prolific Sheep, Fahmy, M.H. (Ed.). CAB International, Wallingford, Oxon, UK
42: FAO, 1987. Production Year Book. Vol. 51. Food and Agricultural Organization of the United Nations, Rome, Italy
43: Faure, M.O., L. Nicol, S. Fabre, J. Fontaine, N. Mohoric, A. McNeilly and C. Taragnat, 2005. BMP-4 inhibits follicle-stimulating hormone secretion in ewe pituitary. J. Endocrinol., 186: 109-121.
CrossRef | Direct Link |
44: Fitch, J., 1989. Booroola Merino. Handbook of Australian Livestock. 3rd Edn., Austalian Meat and Livestock Corporation, Australia
45: Garran, J.C. and L. White, 1985. Merinos, Myths and Macarthurs. Australian National University Press, Australia, pp: 188
46: Ghalsasi, P.M. and B.V. Nimbkar, 1993. The garole-microsheep of bengal, India. Anim. Genetic Res. Inform., 12: 73- 79.
Direct Link |
47: Ghalsasi, P.M., C. Nimbkar and G.D. Gray, 1994. Garole-prolific microsheep of West Bengal, India. Proc. 5th World Cong. Genet. Applied Livest. Prod. Guelph, 20: 456-459.
48: Hailat, N.Q. and S.Q. Lafi, 1998. A deficiency in the slow moving immunoglobulin in awassi sheep. Turk. J. Vet. Anim. Sci., 22: 153-155.
Direct Link |
49: Hanrahan, J.P., 1991. Evidence for Single Gene Effect on Ovulation Rate in the Cambridge and Belclare Breeds. In: Major Genes for Reproduction in Sheep, Elsen, J.M., L. Bodin and J. Thimonier (Eds.). INRA, Paris, pp: 93-102
50: Hanrahan, J.P., S.M. Gergan, P. Mulsant, M. Mullen, G.H. Davis, R. Powell and S.M. Galloway, 2004. Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in cambridge and belclare sheep (Ovis aries). Biol. Reprod., 70: 900-909.
CrossRef | PubMed | Direct Link |
51: Hasnath, M.A., 1980. In Proceedings of SABRAO Workshop on Animal Genetic Resources in Asia and Oceania. Tropical Agriculture Research Centre, Japan, pp: 415-422
Direct Link |
52: Hogan, B.L., 1996. Bone morphogenetic proteins: Multifunctional regulators of vertebrate development. Genes Dev., 10: 1580-1594.
CrossRef | PubMed | Direct Link |
53: Horton, G.M.J. and A. Rodriguez, 1997. Comparison between hair (St. Croix) and wool (Targhee and Dorset) lambs regarding the effect of heat stress on food and water intake, digestive function and nitrogen balance. Archivos-Latinoamericanos-de-Produccion-Anim., 5: 79-92.
54: Jonmundsson, J.V. and S. Adalsteinsson, 1985. Simple Genes for Fecundity in Icelandic Sheep. In: Genetics of Reproduction in Sheep, Land, R.B. and D.W. Robinson (Eds.). Butterworths, London, pp:159-168
55: Juengel, J.L., K.L. Reader, A.H. Bibby, S. Lun, I. Ross, L.J. Haydon and K.P. McNatty, 2006. The role of bone morphogenetic proteins 2, 4, 6 and 7 during ovarian follicular development in sheep: Contrast to rat. Reproduction, 131: 501-513.
56: Juengel, J.L. and K.P. McNatty, 2005. The role of proteins of the transforming growth factor-β superfamily in the intraovarian regulation of follicular development. Human Reprod. Update, 11: 144-161.
57: Kar, K. and C. Prasad, 1992. Recent advances in goat production. Proceedings of the V International Goat Conference held in New Delhi, India during, March 2-8, International Goat Association, New Delhi, pp: 953-969
Direct Link |
58: Kooyman F.N.J., P.J.S. Kooten, J.F. Huntley, A. MacKellar, A.E.C.A. Cornelissen, H.D.F.H. Schallig and P.J.S. Van-Kooten, 1997. Production of a monoclonal antibody specific for ovine immunoglobulin E and its application to monitor serum IgE responses to Haemonchus contortus infection. Parasitology, 114: 395-406.
59: Landmann, W.A., 1960. Inorganic Constituents. In: The Science of Meat and Meat Products, Price, J.F. and B.S. Schweigert (Eds.). W.H. Freeman and Co., San Francisco, California
60: Lanneluc, I., R.D. Drinkwater, J.M. Elsen, D.J. Hetzel and T.C. Nguyen(et al)., 1994. Genetic markers for the Booroola fecundity (Fec) gene in sheep. Mamm. Genome, 5: 26-33.
PubMed | Direct Link |
61: Lanneluc, I., P. Mulsant, N. Saidi-Mehtar and J.M. Elsen, 1996. Synteny conservation between parts of human chromosome 4q and bovine and ovine chromosome 6. Cytogenet Cell Genet., 72: 212-214.
62: Lawrie, R.A. and D.A. Ledward, 2006. Lawries Meat Science. 7th Edn., Woodhead and CRC Press, Cambridge, pp: 229-234
63: Loftus, R. and B. Scherf, 1993. World Watch List for Domestic Animal Diversity. 1st Edn., FAO, Rome, Italy
64: Mason, I.L., 1980. Prolific tropical sheep. Anim. Prod. Health Paper FAO Rome, 17: 124-124.
Direct Link |
65: Mahler, X. and A.K. Lechere, 1998. High prolificacy in Belle-Ile sheep (Brittany-France)-major effects of a putative single gene and a (wh) colour gene on ovulation rate and litter size. Reprod., Nutr. Dev., 38: 473-484.
Direct Link |
66: Mason, I.L., 1988. Sheep a World Dictionary of Livestock Breeds, Types and Varieties. 3rd Edn., CAB International, Wallingform, Oxon, UK
67: Mason, I.L., 1996. Sheep a world dictionary of Livestock Breeds, Types and Varieties. 4th Edn., CAB International, Wallingform, Oxon, UK., pp: 191- 213
68: Massague, J., 1998. TGF-beta signal trunsduction. Annu. Rev. Biochem., 67: 753-791.
69: Mathur, J.N., 2004. Health research policy. ICMR Bull., 34: 49-59.
70: McEwan, J.C. and R.J. Kerr, 1998. Further evidence that major genes affect host resistance to nematode parasites in Coopworth sheep. Wool Technol. Sheep Breeding, 46: 12-16.
Direct Link |
71: McFee, A.E., M.W. Banner and R.L. Murphree, 1965. Chromosome analysis of peripheral leucocytes of the sheep. J. Anim. Sci., 24: 551-554.
72: Medappa, N., 2003. Determinants of the development of food behaviours and nutrition. ICMR Bull., 33: 1-8.
Direct Link |
73: Miresan, V., 2003. Evolution of the main blood indices in Tsigai fattening sheep. J. Central Eur. Agric., 4: 405-410.
Direct Link |
74: Montgomery, G.W., A.M. Crawford, J.M. Penty, K.G. Dodds and A.J. Ede et al., 1993. The ovine Booroola fecundity gene (FecB) is linked to markers from a region of human chromosome 4q. Nature Genet., 4: 410-414.
75: Montgomery, G.W., S.M. Galloway, G.H. Davis and K.P. McNatty, 2001. Genes controlling ovulation rate in sheep. Reproduction, 121: 843-852.
CrossRef | PubMed | Direct Link |
76: Montgomery, G.W., E.A. Lord, J.M. Penty, K.G. Dodds and T.E. Broad et al., 1994. The booroola fecundity (FecB) gene maps to sheep chromosome 6. Genomics., 22: 148-153.
CrossRef | PubMed | Direct Link |
77: Montgomery, G.W., J.M. Penty, E.A. Lord and M.F. Broom, 1995. The search for the Booroola (FecB) mutation. J. Reprod. Fert., 49: 113-121.
78: Montgomery, G.W., J.M. Penty, E.A. Lord, J. Brooks and A.S. McNeilly, 1995. The gonadotropin releasing hormone receptor maps to sheep Chromosome 6 outside of the region of the FecB locus. Mamm. Genome, 6: 436-438.
79: Mukhamedgaliev, E.M., V.F. Saritskii, I.V. Sharipov and R. Zhapbasov, 1974. Some data on the karyotype of Kazakh sheep. Trudy Inst. Exp. Noi Biol. Akad. Nauk Kazahoshoi, 10: 3-12.
80: Mulsant, P., F. Lecerf, S. Fabre, L. Schibler and P. Monget et al., 2001. Mutation in bone morphogenetic protein receptor-IB is associated with increased ovulation rate in Booroola Merino ewes. Proc. Natl. Acad. Sci. USA., 98: 5104-5109.
CrossRef | Direct Link |
81: Murray, J. and W.D. Smith, 1994. Ingestion of host immunoglobulin by three non-blood-feeding nematode parasites of ruminants. Res. Vet. Sci., 57: 387-389.
82: Nilsson, E.E. and M.K. Skinner, 2003. Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol. Reprod., 69: 1265-1272.
Direct Link |
83: Nimbkar, C., 2002. Gains from garole the wonder sheep of West Bengal. Partners Res. Dev. ACIAR, 15: 31-36.
Direct Link |
84: Nimbkar, C., P.M. Ghalsasi, B.S.W. Walkden, L.P. Kahn, G.D. Gray and G.M. Stone, 2000. A comparison of the growth performance and worm resistance of lambs produced by diallel crossing of three Indian sheep breeds. J. Anim. Sci., 13s: 72-75.
85: Nimbkar, C., P.M. Ghalsasi, R.R. Ghatge and G.D. Gray, 1998. Establishment of prolific Garole sheep from West Bengal in the semi-arid deccan plateau of Maharashtra. Proc. 6th World Cong. Genet. Applied Livestock Prod. Armidale, 25: 257-260.
86: De Oliveira Filho, E.B., 1978. A contribution to the study of karyotypes in the domestic sheep (Onis aries). L. Revista da Faculdada de Medicina Veterinariae Zootechria da Universidode de Sao Paulo, 15: 201-204.
87: Otsuka, F., R.K. Moore and S. Shimasaki, 2001. Biological function and cellular mechanism of bone morphogenetic protein-6 in the ovary. J. Biol. Chem., 276: 32889-32895.
88: Owen, J.B., C.J. Whitaker, R.E.F. Axford and I.A. Dewi, 1990. Expected consequences of the segregation of a major gene in a sheep population in relation to observations on the ovulation rate of a flock of Cambridge sheep. Anim. Prod., 51: 277-282.
89: Pal, U.K., M.K. Agnihotri and N.K Sinha, 1997. Carcass traits of Muzaffarnagari lambs under intensive and semi-intensive management systems. Indian J. Anim. Sci., 67: 720-722.
Direct Link |
90: Pan, S. and A.K. Sahoo, 2003. Garole Sheep, Report of Ad-Hoc Research Scheme on Survey Evaluation of Garole Sheep in Sundarban Area of West Bengal. WBUAFS, Mohanpur, West Bengal
91: Pan, S., A.K. Sahoo, M.S. Tantia and S.P.S. Ahlawat, 2004. Garole Sheep, NATP (MM) on Animal Genetic Resource Bio-Diversity. WBUAFS, Mohanpur and Kolkata, West Bengal and NBAGR, Karnal, Haryana, India
92: Pardeshi, V.C., M.N. Sainani, J.F. Maddox, P.M. Ghalsasi and P.M. Ghalsasi et al., 2005. Assessing the role of FecB mutation in productivity of Indian sheep. Curr. Sci., 89: 887-890.
Direct Link |
93: Pepin, B.M., A.O. Vaiman, B. Vigier, F. Piumi, E. Cribiu and C. Cotinot, 2003. Expression profiles and chromosomal localization of genes controlling meiosis and follicular development in the sheep ova. Biol. Reprod., 68: 985-995.
94: Piper, L.R. and B.M. Bindon, 1982. Genetic segregation for fecundity in booroola merino sheep. Proc. World Cong. Sheep Beef Cattle Breed., 1: 394-400.
95: Pierre, A., C. Pisselet, J. Dupont, B.P. Mandon, D. Monniaux, P. Monget and S. Fabre, 2004. Molecular basis of bone morphogenetic protein-4 inhibitory action on progesterone secretion by ovine granulosa cells. J. Mol. Endocrinol., 33: 805-817.
96: Piper, L.R. and B.M. Bindon, 1982. The Booroola Merino and the Performance of Medium Non-peppin Crosses at Armidale. In: The Booroola Merino, Piper, L.R., B.M. Bindon and R.D. Nethery (Eds.). CSIRO, Melbourne, pp: 9-19
97: Piper, L.R., B.M. Bindon, 1996. The Booroola Merino. In: Prolific Sheep, Fahmy M.H. (Ed.). CAB International, Wallingford, UK., pp:152-160
98: Prasad, J., 1996. Goat, Sheep and Pig Production and Management. 1st Edn., Kalyani Publishers, New Delhi, pp: 151-163
99: Prasad, J., 1997. Goat, Sheep and Pig-Production and Management. Kalyani Publishers, New Delhi
100: Radomska, M.J., E. Martyniuk, J. Klewiec and A. Knothe, 1988. Inheritance of high prolificacy of the Olkuska sheep (preliminary results). J. Agric. Sci., 60: 597-598.
101: Rakshit, A., P.K. Senapati and R. Duttagupta, 1999. Study of metaphase chromosome in sheep. J. Interacad, 3: 309-312.
102: Rcheulishvili, M.D. and T.A. Dzhokhaze, 1985. Akaryological study of Imeritian sheep. Soobshch. Akad. Nauk. Gruz, 117: 585-588.
103: Rice, E.E., 1971. The Nutritional Content and Value of Meat and Meat Products. In: The Science of Meat and Meat Products, Price, J.F. and B.S. Schweigert (Eds.). W.H. Freeman and Co., San Francisco, Calif
104: Roy, P.K., G.R. Pattanayak, and B.N. Patro, 1991. Karyotyping of local indigenous sheep. Orissa Vet. J., 16: 29-33.
105: Ruiz-de-la-Torre, J.L., A. Velarde, A. Diestre, M. Gispert, S.J.G. Hall, D.M. Broom and X. Manteca, 2001. Effects of vehicle movements during transport on the stress responses and meat quality of sheep. Vet. Record, 148: 227-229.
106: Sahana, G., S.C. Gupta and A.E. Nivsarkar, 2001. Garole: The prolific sheep of India. Anim. Genet. Resour. Inf., 31: 55-63.
107: Sahoo, A.K. and S. Pan, 2002. Annual Report, NATP Project on Characterization and Conservation of Bengal Goat and Garole Sheep. WBUAFS, Kolkata, West Bengal
108: Seaton, D.S., T.J. O'Meara, R.A. Chandler and R.M. Sandeman, 1992. The sheep antibody response to repeated infection with Lucilia cuprina. Int. J. Parasitol., 22: 1169-1174.
109: Shackelford, S.D., K.A. Leymaster, T.L. Wheeler and M. Koohmaraie, 2005. Lamb meat quality progress report number 1. Preliminary results of an evaluation of effects of breed of sire on carcass composition and sensory traits of lamb. http://www.ars.usda.gov/sp2UserFiles/Place/54380530/Publications/LambMeatQualityReportNumber1.pdf.
110: Sharma, R.C., A.L. Arora, H.K. Narula and R.N. Singh, 1999. Characteristics of garole sheep in India. AGRI, 26: 57-64.
111: Shimasaki, S., R.K. Moores, F. Otsuka and G.F. Erickson, 2004. The bone morphogenetic protein system in mammalian reproduction. Endocrine Rev., 25: 72-101.
Direct Link |
112: Shimasaki, S., R.J. Zachow. D. Li, H. Kim and S. Lemura et al., 1999. A functional bone morphogenetic protein system in the ovary. PNAS, 96: 7282-7287.
Direct Link |
113: Shirinskii, M.A., K.I. Mamin and U.T. Drofev, 1982. Morphology and the linear parameters of chromosomes of black karakul ewes of the Persian Pelt type. Shonik Nanchnykh Stalii Kazakhskogo Nanhno Issledovatel's Kogo Instituta Karakulevodstva, 7: 31-38.
114: Singh, R.N., 1998. Method of Slaughter. Essential of Animal Production and Management, Edn., Kalyani Publishers, New Delhi, pp: 463 - 466
115: Singh, R.N., 2000. Conservation and management of sheep genetic resources. Proceedings of the National Workshop on Conservation and Management of Genetic Resources of Livestock, (CMGRL'00), National Academy of Agricultural Sciences, New Delhi, GOI, GBPUA and T, Pantnagar, India, pp:170-180
116: Singh, R.N. and S.D.J. Bohra, 1996. Garole sheep: A profile (Bengal breed of sheep locally known as garole). Indian J. Small Ruminants, 2: 38-42.
Direct Link |
117: Singh, R.A., 1997. Technology of Wool Production and Management. Kalyani Publishers, New Delhi
118: Smuts, S., L. Hunter and M. van Rensburg, 2001. The role of sheep breed and mohair style and character in the OFDA curvature vs. staple crimp/wave frequency relationship. Wool Technol. Sheep Breed., 49: 53-61.
Direct Link |
119: Sodhi, M., M. Mukesh, R. Arora, M.S. Tantia and S. Bhatia, 2003. Genetic characterization of garole sheep using microsatellite markers. Indian J. Dairy Sci., 56: 167-173.
Direct Link |
120: Turner, H.N., 1980. Origin of the CSIRO Booroola. Proceedings of the Workshop on The Booroola Merinos held on, Aug. 24-25, Armidale, N.S.W. Melbourne, Australia, pp: 1-7
121: Turner, H.N., 1982. The Booroola Merinos. In: Merino Improvement Programs in Australia, Piper, L.R., B.M. Bindon and R.D. Nethery (Eds.). CSIRO, Melbourne, Australia
122: Turner, H.N., 1983. Origin of the CSIRO booroola in the booroola merinos. Wool Technol. Sheep Breed., 31: 10-13.
123: Vazir, S., 2003. Determinants of the development of food behaviours and nutrition. ICMR Bull., 33: 1-8.
124: Waelchli, R.O., C. Muller, M. Hassig and P. Rusch, 1994. Immunoglobulin concentrations in colostrum and serum of lambs of dairy sheep breeds. Vet. Record, 135: 16-17.
125: Walling, G.A., K.G. Dodds, S.M. Galloway, A.E. Beattie and E.A. Lord et al., 2000. Characterisation and mapping of the Booroola (FecB) gene using regression analysis in sheep. Proceedings of the British Society of Animal Science, March 2006, New York, UK., pp: 41-41
126: Walling, G.A., K.G. Dodds, S.M. Galloway, A.E. Beattie and E.A. Lord et al., 2000. The consequences of carrying the Booroola fecundity (FecB) gene on liveweight. Proceedings of the British Society of Animal Science, (BSAS`00), New York, UK., pp: 43-43
127: Watt, B.K. and A.L. Merrill, 1963. Composition of Foods-Raw, Processed and Prepared. U.S. Dept. of Agriculture, Washington
128: White, G.P., E.N.T. Meeusen and S.E. Newton, 2001. A single-chain variable region immunoglobulin library from the abomasal lymph node of sheep infected with the gastrointestinal nematode parasite Haemonchus contortus. Vet. Immunol. Immunopathol., 78: 117-129.
129: Woolaston, R.R. and G.D. Gray, 1991. Potential for improving genetic resistance to sheep diseases. Wool Technol. Sheep Breed., 39: 84-87.
Direct Link |
130: Wilson, T., X.Y. Wu, J.L. Juengel, I.K. Ross and J.M. Lumsden et al., 2001. Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein ib receptor (alk-6) that is expressed in both oocytes and granulosa cells. Biol. Reprod., 64: 1225-1235.
CrossRef | PubMed | Direct Link |
131: Xia, Y., T. O'Shea, R. Murison and J.R. McFarlane, 2003. Concentrations of progesterone, follistatin and follicle-stimulating hormone in peripheral plasma across the estrous cycle and pregnancy in merino ewes that are homozygous or noncarriers of the booroola gene. Biol. Reprod., 69: 1079-1084.
132: Yi, S.E., P.S. Lapolt, B.S. Yoon, J.Y.C. Chen, J.K.H. Lu and K.M. Lyons, 2001. The type I BMP receptor Bmpr IB is essential for female reproductive function. PNAS, 98: 7994-7999.
133: Zhang, Y.D., G.D. Gray and B.J. Crook, 1998. Genetic enhancement of resistance to gastrointestinal worm infection in crossbred maternal genotypes used for meat sheep production in Australia. Proc. 6th World Cong. Genet. Applied Livest. Prod., 27: 315-318.
Direct Link |
134: Banerjee, S. and S. Banerjee, 2000. Garole sheep of Bengal. Asian Livestock, 24: 19-21.
135: Galloway, S.M., K.P. McNatty, L.M. Cambridge, M.P.E. Laitinen and J.L. Juengel et al., 2000. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet., 25: 279-283.
CrossRef | PubMed | Direct Link |