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Effect of temperature on incubation period, embryonic mortality, hatch rate, egg water loss and partridge chick weight (Rhynchotus rufescens)

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The aim of this study was to determine the effects of incubation temperature (34.5; 35.5; 36.5; 37.5 and 38.5ºC), on incubation period, embryonic mortality, hatching rate, water loss and chick weight at hatch, using daily incubation of partridge (Rhynchotus rufescens) eggs. The highest hatching percentage was obtained between 35.5 and 36.5ºC. Incubation length and temperature were inversely proportional. Water loss was lower in eggs incubated at low temperatures as compared to high temperatures. There was no difference among incubation temperatures in absolute and relative hatchling weights. Early embryonic mortality increased at low temperatures (<35.5ºC), whereas intermediate and late embryonic mortality increased at high temperatures (>36.5ºC). Our results show that, under conditions of daily incubation of eggs in the same incubator, higher hatching rate can be obtained using temperatures between 35.5ºC and 36.5ºC; incubation temperature is inversely proportional to incubation length, and absolute and relative weights of partridge chicks are not affected by incubation temperature.
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Brazilian Journal of Poultry Science
Revista Brasileira de Ciência Avícola
ISSN 1516-635X May - Aug 2003 / v.5 / n.2/ 131 - 135
131
Effect of Temperature on Incubation Period,
Embryonic Mortality, Hatch Rate, Egg Water Loss
and Partridge Chick Weight (Rhynchotus rufescens)
Isabel Cristina Boleli
Departamento de Morfologia e Fisiologia
Animal
Universidade Estadual Paulista, Faculdade de
Ciências Agrárias e Veterinárias
Via de Acesso Prof. Paulo Donato Castellani,
Km 5
Jaboticabal , SP  Brasil
14874-900
E-mail: icboleli@fcav.unesp.br
Mail Address
Keywords
Nakage ES
Cardozo JP
Pereira GT
Queiroz SA
Boleli IC
Faculdade de Ciências Agrárias e Veterinárias
UNESP- Jaboticabal.
Author(s)
Arrived: july 2002
Approved: march 2003
ABSTRACT
The aim of this study was to determine the effects of incubation
temperature (34.5; 35.5; 36.5; 37.5 and 38.5oC), on incubation period,
embryonic mortality, hatching rate, water loss and chick weight at hatch,
using daily incubation of partridge (Rhynchotus rufescens) eggs. The
highest hatching percentage was obtained between 35.5 and 36.5oC.
Incubation length and temperature were inversely proportional. Water
loss was lower in eggs incubated at low temperatures as compared to
high temperatures. There was no difference among incubation
temperatures in absolute and relative hatchling weights. Early embryonic
mortality increased at low temperatures (<35.5oC), whereas intermediate
and late embryonic mortality increased at high temperatures (>36.5oC).
Our results show that, under conditions of daily incubation of eggs in
the same incubator, higher hatching rate can be obtained using
temperatures between 35.5oC and 36.5oC; incubation temperature is
inversely proportional to incubation length, and absolute and relative
weights of partridge chicks are not affected by incubation temperature.
INTRODUCTION
Temperature is one of the physical factors that determine the success
of incubation. Therefore, it is essential to determine and use a
temperature that promotes the highest hatchability (Swann & Brake,
1990b; French, 1997) and the best hatchling quality (Wilson, 1991;
Decuypere & Mitchels, 1992), known as optimum incubation
temperature.
The optimum incubation temperature of wild fowl eggs is within a
wide range of values, varying from 33oC to 39oC, whereas a narrower
range (37oC to 38oC) is considered as optimum for domestic poultry
(Visschedijk, 1991).
The effect of incubation temperature on egg hatchability and hatchling
quality may be related to its influence on incubation length and water
loss during incubation. However, such effects depend on how long and
how intense is the shift from optimum temperature. According to Givisiez
et al. (2000) an increase of 1oC (38.8oC) above the optimum incubation
temperature (37.8oC) starting at day 13 of incubation causes a significant
reduction of the hatching rate of broiler eggs, whereas such effect is
not observed when the temperature is reduced in 1oC (36.8oC).
Incubation temperature correlates directly to the duration of in ovo
development both in turkeys (French, 1994) and broilers (Byerly, 1938;
Decuypere et al., 1979). The development is delayed in temperatures
below optimum and accelerated in temperatures above optimum
(Romanoff, 1960; Wilson, 1991). Such difference in embryo development
rate as a result from changing the incubation temperature seems to
explain body weight differences reported by some authors (Givisiez et
Incubation, hatchability, mortality,
temperature, water loss.
Acknowledgment
The authors thank the Wild Animal Sector of
FCAV - UNESP/ Jaboticabal, for the partridge
eggs, and CNPq for M. Sc. scholarship granted
to E.S.N.
Nakage ES, Cardozo JP, Pereira GT,
Queiroz SA, Boleli IC
Effect of Temperature on Incubation Period, Embryonic
Mortality, Hatch Rate, Egg Water Loss and Partridge Chick
Weight (Rhynchotus rufescens)
132
al., 2000; Decuypere et al., 1979; Swan & Brake,
1990a).
Water loss is a normal process during incubation,
usually 12 to 14% of water is lost in broilers and turkeys
eggs (Rahn et al., 1981). However, too low or too high
water loss influences embryo development (Rahn & Ar,
1974), and consequently, egg hatchability (Meir et al.,
1984). Incubation temperatures above the optimum
cause excessive egg water loss (higher than 14%),
leading to embryo mortality by dehydration. On the
other hand, temperatures below the optimum
decrease hatchability due to reduced water loss (<
12%), which causes an over-hydration of the embryo
and an impairment of gas exchange (Romanoff, 1930).
The partridge (Rhynchotus rufescens) is a wild bird
that has significantly reduced natural populations
nowadays due to predatory hunting and destruction
of natural habitats. Some poultry producers have shown
increasing interest in raising partridges commercially
as an alternative source of exotic meat. However,
there is little information in literature regarding egg
incubation parameters for this specie.
One of the major problems in partridge production
is the low egg production, which is due to the short
laying period (6 months; spring and summer). In addition,
this species is undergoing the first stages of taming
process, and therefore, it is still not well adapted to
captivity conditions. Thus, with the objective of
determining adequate handling of fertile eggs and also
to increase partridge chick production, the present study
analyzed the effects of incubation temperature on
incubation length, water loss, embryonic mortality, hatching
rate, as well as on the weight of the chick partridge by
using daily egg incubation in a same incubator.
MATERIAL AND METHODS
Eggs and incubation
In the present study, 182 fertile eggs (56 ± 3g) were
collected (3 times/day) during the intermediate laying
period (November-December/2001) from partridges
(Rhynchotus rufescens) given pelleted diet (15% crude
protein, 2,800 kcal ME/kg) and water ad libitum. All
eggs were manually sprayed using a disinfecting
solution of 1% formaldehyde + 0.5% quaternary
ammonium (Branco, 1990; Morita, 1990). After drying,
2 to 4 eggs were transferred to incubators (Premium
Ecológica, Model IP120) three times per day until a
maximum of 65 eggs per incubator.
On day 16 of incubation, eggs were weighed and
transferred to hatchers (Premium Ecológica, Model
NP120). Temperature and relative humidity in the
incubators and hatchers were monitored and recorded
3 times/day by direct observation of dry and wet bulb
thermometers, respectively, throughout the incubation
period.
Eggs were divided into five experimental groups
with different incubation temperatures: group 1
(34.5oC, N: number of fertile eggs=26), group 2 (35.5oC,
N=40), group 3 (36.5oC, N=62), group 4 (37.5oC, N=31),
and group 5 (38.5oC, N=23). All groups were submitted
to the same relative humidity (60%) until hatching.
Parameters
The following parameters were analyzed for each
experimental group: hatching percentage (number of
hatched eggs/total number of incubated fertile eggs x
100); percentage of water loss up to the transference
to the hatcher [(egg weight before incubation  egg
weight at transference)/egg weight before incubation
x 100]; total incubation period (days); absolute and
relative hatchling weight (absolute chick weight/egg
weight before incubation x 100); total mortality rate
[(number of incubated fertile eggs  number of hatched
eggs)/number of incubated fertile eggs x 100]. Non-
hatched eggs were opened and embryo stage was
determined according to Hamburger & Hamilton (1951).
Then, it was determined early mortality rate (number of
embryos dead between 1 and 7 days/number of
incubated fertile non-hatched eggs x 100); intermediate
mortality rate (number of embryos dead between 8 and
15 days/number of incubated fertile non-hatched eggs
x 100) and late mortality rate (number of embryos dead
between 16 days and hatching/number of incubated
fertile non-hatched eggs x 100).
Statistical analysis
Data were submitted to one-way analysis of
variance (temperature) and subsequently expressed by
polynomial functions to justify the differences between
the treatment means. Mortality data were evaluated
by Fishers Test (5%). All statistical analysis were
performed using GLM procedure of SAS (Statistical
Analysis System, 1998).
RESULTS AND DISCUSSION
Figure 1 shows a significant (p<0.05) quadratic
effect for hatchability as a function of incubation
temperature (y= -7970 + 450.5x  6.312x2; R2= 0.998),
thus the highest hatching rate was observed within
the temperature range of 35.5oC and 36.5oC.
Nakage ES, Cardozo JP, Pereira GT,
Queiroz SA, Boleli IC
Effect of Temperature on Incubation Period, Embryonic
Mortality, Hatch Rate, Egg Water Loss and Partridge Chick
Weight (Rhynchotus rufescens)
133
The optimum incubation temperature depends on
the avian species. The best hatchability is obtained at
37.8oC for broilers (Barott, 1937), 37.2oC  37.5oC for
quails (Albino & Neme, 1998),39.0oC  39.5oC for
waterfowl and 38.3oC  38.6oC for turkey (Reis,
1942a,b),39.0oC for ducks and 39.5oC for geese
(Cullington, 1975). Moreng & Avens (1990) reported
that the best hatchability for European partridges was
found at an incubation temperature of 37.4 oC. Thus,
our findings also suggest that the optimum incubation
temperature is lower for wild birds when compared
to domestic birds.
The mortality of partridge eggs (Figure 1) was also
described by a quadratic effect as a function of
incubation temperature (y= 8070  450.5x + 6.312x2;
R2= 0.998). According to this equation, opposite to
what happens to hatching rate, temperatures below
34.5oC and above 36.5oC increase mortality. However,
incubation at a temperature lower than 35.5 o
C
increased late mortality, whereas incubation at a
temperature above 36.5oC showed predominantly
early and intermediate mortality (Figure 2). These data
differ from that reported for broilers, since broiler
embryos are more sensitive to temperatures below
optimum (37.8oC) in the beginning of incubation
(French, 1997), and to temperatures above optimum
during late incubation period (Ono et al., 1994).
Primmett et al. (1988) also reported that embryo survival
was lower at early stages of development when
incubation temperature is set to at extremes of the
temperature range. Thus, our findings revealed that
the partridge embryo is also susceptible to incubation
temperature, but mortality at early stages is higher at
low temperatures, differing from broiler embryos.
In the present study, incubation of partridge eggs
lasted 26 and 19 days at 34.5oC and 38.5oC,
respectively. Within this range of temperature, the
incubation period of partridge eggs changes as a
function of incubation temperatures (y= 674.7  34.21x
+ 0.4464x2; R2= 0.968) (Figure 3). French (1994) also
observed in turkeys that incubation time is reduced as
incubation temperature increases, showing that this is
a common feature in different bird specie.
33.5 34.5 35.5 36.5 37.5 38.5 39.5
10
30
50
70
90
y= -7970+450.5x - 6.312x 2
R2= 0.998
y= 8070-450.5x + 6.312x 2
R2= 0.998
10
30
50
70
90
Incubation temperature (oC)
Hatching (%)
Mortality (%)
Figure 1  Hatching (¡) and mortality (
) rates of partridge eggs
according to incubation temperatures.
Figure 2  Early, intermediate, late and total mortality (%) during
the incubation of partridge eggs under different temperatures.
Number above the bar corresponds to number of non-hatched
eggs.
33.5 34.5 35.5 36.5 37.5 38.5
17
19
21
23
25
27
y= 674.7 - 34.21x + 0.4464x2
R2= 0.968
Temperatura de incuba
ç
ão (oC)
Incubation time (days)
Figure 3  Incubation period length of partridge eggs according
to incubation temperatures. N=20/temperature.
The plasticity of broiler embryos to respond to shifts
in incubation temperature, which might delay or
accelerate their development, may be used in
19
16
23
13
11
0
10
20
30
40
50
60
70
80
90
34.5 35.5 36.5 37.5 38.5
Incubation temperature ( oC)
Mortality (%)
Early Intermediate Late Total
Nakage ES, Cardozo JP, Pereira GT,
Queiroz SA, Boleli IC
Effect of Temperature on Incubation Period, Embryonic
Mortality, Hatch Rate, Egg Water Loss and Partridge Chick
Weight (Rhynchotus rufescens)
134
hatcheries as a means to manipulate hatching rate.
Nevertheless, such technique must be carefully
considered for partridges, since data presented here
evidenced that incubation temperatures below 34.5oC
and above 36.5oC result in a significant decrease in
hatching rate, opposite to the main objective of the
incubation process, which is to maximize hatching. The
risk of using such procedure to manipulate hatching
day in broilers was already mentioned by Wilson (1990).
Therefore, incubation length or hatching day must be
analyzed simultaneously with the hatchability of fertile
eggs, because optimum incubation temperature is
determined by their synchronism (Visschedijk, 1991).
With respect to water loss percentage in partridge
eggs, there was a quadratic effect as a function of
incubation temperatures from day 1 to day 16 of
incubation (y= -50.5 + 2.797x  0.037x2; R2= 0.891),
that is, the higher the temperature, the higher the
percentage of egg water loss (Figure 4). Similar effects
of incubation temperature on water loss were reported
in broiler eggs by Swann & Brake (1990b).
Results showed that water loss during the first 16
days of incubation was approximately 8% of the initial
weight of partridge eggs incubated at 35.5oC and
36.5oC, and 9.94% when incubated at 37.5oC. These
values are similar to water loss for broilers eggs (10.8%
at 37.8oC) (Deeming, 1993). Water loss of partridge
eggs incubated at 34.5oC was lower when compared
to eggs incubated at higher temperatures (Figure 4),
which suggests that chicks hatched at 34.5ºC would
be heavier than those hatched at higher temperatures,
considering that water percentage in the albumen
determines chick weight at hatching (Simkiss, 1980).
However, as shown in Figure 5, there was no significant
difference between the incubation temperatures for
chick weight, showing that incubation temperature
and, consequently, water loss in the first 16 days of
incubation did not influence absolute and relative chick
weights in partridge. Data shown in Figures 4 and 5
suggest that possibly all partridge eggs may lose the
same percentage of water (p>0.05) until the end of
incubation. Thus, in such case, incubation temperature
may influence the velocity of water loss, but not the
total percentage of water loss. Swann & Brake (1990a)
also did not report effects of incubation temperature
on the weight of broiler hatchlings.
The relative weight of partridge chick was about
72.3 to 73.14% of the weight of fresh eggs (Figure 5).
A broader variation (62 to 71%) was found in broiler
chick (Merritt & Gowe, 1965). The smaller variation in
the relative weight of partridge chicks compared to
broiler chicks may be related to a higher uniformity of
egg weight in the present study.
In summary, the present study shows that, when
partridge eggs (Rhynchotus rufescens) are incubated
daily in the same incubator, the highest hatching rate
is obtained at 35.5oC and 36.5oC. Incubation
temperature is inversely proportional to incubation
length, the higher incubation temperature, the higher
the rate of egg water loss in the first 16 days of
incubation. Also, it was shown that absolute and
33.5 34.5 35.5 36.5 37.5 38.5
1.50
1.75
2.00
2.25
2.50
y= -50.50 + 2.797x - 0.037x2
R2= 0.891
Incubation temperature (oC)
Water loss (log%)
Figure 4  Effect of different incubation temperatures on total
water loss (log %) of partridge eggs, from day 1 to day 16 of
incubation. N=20/temperature.
33.5 34.5 35.5 36.5 37.5 38.5 39.5
30
40
50
60
70
80
30
40
50
60
70
80
Incubation temperature (oC)
Absolute weight (g)
Relative weight (%)
Figure 5  Absolute (
) and relative (¡) weight of partridge
hatchlings after incubation under different temperatures. (Each
dot represents mean ± SD; N=20/temperature).
Nakage ES, Cardozo JP, Pereira GT,
Queiroz SA, Boleli IC
Effect of Temperature on Incubation Period, Embryonic
Mortality, Hatch Rate, Egg Water Loss and Partridge Chick
Weight (Rhynchotus rufescens)
135
relative weights of partridge chicks are not affected
by incubation temperature, and that temperature
below 35.5ºC result in late mortality, whereas
temperatures above 36.5oC causes an increase in early
and intermediate mortality.
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... Embryonic development and egg water-loss are also linked to ambient air temperature (Nakage et al., 2003). Water around the nest is hence important for successful development of the embryo and in increasing hatching success. ...
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Cleidoic eggs possess very efficient and orchestrated systems to protect the embryo from external microbes until hatch. The cuticle is a proteinaceous layer on the shell surface in many bird and some reptile species. An intact cuticle forms a pore plug to occlude respiratory pores and is an effective physical and chemical barrier against microbial penetration. The interior of the egg is assumed to be normally sterile, while the outer eggshell cuticle hosts microbes. The diversity of the eggshell microbiome is derived from both maternal microbiota and those of the nesting environment. The surface characteristics of the egg, outer moisture layer and the presence of antimicrobial molecules composing the cuticle dictate constituents of the microbial communities on the eggshell surface. The avian cuticle affects eggshell wettability, water vapor conductance and regulates ultraviolet reflectance in various ground-nesting species; moreover, its composition, thickness and degree of coverage are dependent on species, hen age, and physiological stressors. Studies in domestic avian species have demonstrated that changes in the cuticle affect the food safety of eggs with respect to the risk of contamination by bacterial pathogens such as Salmonella and Escherichia coli. Moreover, preventing contamination of internal egg components is crucial to optimize hatching success in bird species. In chickens there is moderate heritability (38%) of cuticle deposition with a potential for genetic improvement. However, much less is known about other bird or reptile cuticles. This review synthesizes current knowledge of eggshell cuticle and provides insight into its evolution in the clade reptilia. The origin, composition and regulation of the eggshell microbiome and the potential function of the cuticle as the first barrier of egg defense are discussed in detail. We evaluate how changes in the cuticle affect the food safety of table eggs and vertical transmission of pathogens in the production chain with respect to the risk of contamination. Thus, this review provides insight into the physiological and microbiological characteristics of eggshell cuticle in relation to its protective function (innate immunity) in egg-laying birds and reptiles.
... The incubation temperature is an essential factor for a normal development of broiler chicken embryos (Gallus gallus domesticus) (Nakage et al. 2003, Lourens et al. 2006, Wineland et al. 2006, Yalçin et al. 2007. Eggs incubated at temperatures higher than the standard conditions have severe effects on the physiology and development of broiler chicken embryos (French 1997). ...
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The increased incubation temperature has several impacts on the physiology and development of broiler chicken embryos. However, the impact of these conditions on embryonic immunity is unclear. The aim of this study is to evaluate the effect of intermittent thermal manipulation during embryogenesis (TM) on the mRNA expression of cytokines in the spleen of chicken embryos. In this study, the IL-4, IL-6, IL-8, IL-15, IL-16, IL-17, IL-18, IFN-γ, IFN-β, IFN-α, TNF-α and IL-1β genes are evaluated. The eggs of the TM group were subjected to thermal manipulation at 39oC and 65 % relative humidity for eighteen hours/day during embryonic days (ED) 10-18, whereas the eggs of the control group were kept at 37.8oC and 56 % RH throughout the incubation period. On ED 18, the spleen was collected from the embryos in order to evaluate the mRNA levels of cytokines by relative quantitation real time RT-PCR. On the day of hatching, the hatchability rate, body weight, and cloacal temperature (Tc) of the hatched chicks were recorded. TM significantly increased the mRNA expression of IL-6, IL-8, IL-4, IL15, IL-16, IL-17, IL-18, IFN-γ, IFN-β, IFN-α, TNF-α and IL-1β in the spleen of broiler chicken embryos on ED eighteen. However, TM did not significantly affect the hatchability rate, Tc and the body weight of chicks on the day of hatching. In conclusion, results of the present study suggest that TM modulates the cytokine expression in broiler embryos, but did not lead to significant impacts on the hatchability rate and hatchling body weights, and cloacal temperatures. (7) (PDF) Thermal Manipulation during Broiler Chicken Embryogenesis Modulates the Splenic Cytokines' mRNA Expression. Available from: https://www.researchgate.net/publication/337901879_Thermal_Manipulation_during_Broiler_Chicken_Embryogenesis_Modulates_the_Splenic_Cytokines'_mRNA_Expression [accessed Dec 11 2019].
... The incubation temperature is an essential factor for a normal development of broiler chicken embryos (Gallus gallus domesticus) (Nakage et al. 2003, Lourens et al. 2006, Wineland et al. 2006, Yalçin et al. 2007. Eggs incubated at temperatures higher than the standard conditions have severe effects on the physiology and development of broiler chicken embryos (French 1997). ...
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Full-text available
The increased incubation temperature has several impacts on the physiology and development of broiler chicken embryos. However, the impact of these conditions on embryonic immunity is unclear. The aim of this study is to evaluate the effect of intermittent thermal manipulation during embryogenesis (TM) on the mRNA expression of cytokines in the spleen of chicken embryos. In this study, the IL-4, IL-6, IL-8, IL-15, IL-16, IL-17, IL-18, IFN-γ, IFN-β, IFN-α, TNF-α and IL-1β genes are evaluated. The eggs of the TM group were subjected to thermal manipulation at 39 o C and 65 % relative humidity for eighteen hours/day during embryonic days (ED) 10-18, whereas the eggs of the control group were kept at 37.8 o C and 56 % RH throughout the incubation period. On ED 18, the spleen was collected from the embryos in order to evaluate the mRNA levels of cytokines by relative quantitation real time RT-PCR. On the day of hatching, the hatchability rate, body weight, and cloacal temperature (T c) of the hatched chicks were recorded. TM significantly increased the mRNA expression of IL-6, IL-8, IL-4, IL15, IL-16, IL-17, IL-18, IFN-γ, IFN-β, IFN-α, TNF-α and IL-1β in the spleen of broiler chicken embryos on ED eighteen. However, TM did not significantly affect the hatchability rate, T c and the body weight of chicks on the day of hatching. In conclusion, results of the present study suggest that TM modulates the cytokine expression in broiler embryos, but did not lead to significant impacts on the hatchability rate and hatchling body weights, and cloacal temperatures.
... So, concerns were raised in terms of EMF impact on human embryos and newborn infants [25]. It was not taken into account that chicken embryos in an incubator are static and thermally insulated, being at the same time very vulnerable to heat [93]. The temperature inside eggs may be elevated with damaged hot spots. ...
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... Thus, incubator device can help farmers to hatch an egg to produce the chicken on a big number [1]. Researchers have to build the incubator for various egg, such as for Chicken [2], quail [3], Turtle [4], Partridge [5], and other. For the incubating system, researchers developed the incubator to automate the adjustment system, such as the temperature [6], humidity [2], egg reversal [7], and other [8] [9] which based on the microcontroller [10] [8], IoT [10] [11], and other [12]. ...
... Hatching temperature above optimum point will cause water loss that is excess in egg (higher from 14%), which led to embryonic death due to dehydration [8]. On the other hand, temperature under optimum point will reduce hatchery rate for purpose lowering rate of water loss < 12%, cause gas exchange decline [9]. Figure 3: Moving floor type egg turning Egg turning method as in Figure 3 widely used in incubation machine that is small scale. ...
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Poultry is one of the most consumed agricultural produce in Ghana. Because of this high demand, the problem necessitates efforts to maximize the yield of poultry production in the country. Relying on natural means of hatching eggs to increase poultry production is inefficient thus the need for technologies that will aid in maximizing the yield. Artificial means of solving this problem have brought about the invention of the incubator. Although this has helped in large-scale incubation, incubators in the market are very expensive which makes Ghanaian poultry farmers find it difficult to purchase. This project investigates the design and implementation of an affordable, automated incubator for local poultry farmers. It is aimed at designing a low-cost smart incubator to ensure the maintenance of the optimum environmental conditions necessary for hatching eggs. These conditions: Ventilation, Temperature, Relative Humidity, regular positioning, and eggs turnings are kept at their optimal values to efficiently increase the hatchability rate. Temperature and humidity sensors are used to read temperature and humidity values inside the incubator respectively. These values are sent to a microcontroller which then coordinates other parts of the incubator to execute automated tasks. A mobile application is integrated with the incubator for the communication of important information to the poultry farmer.
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