Y. Piestun1,2, O. Halevy2 and S. Yahav1
1Department of Poultry and Aquaculture Sciences, ARO the Volcani Center, , P.O. Box 6, Bet-Dagan 50250, Israel ; Questo indirizzo email è protetto dagli spambots. E' necessario abilitare JavaScript per vederlo. ; 2Dept. of Animal Sciences, Faculty of Agriculture, the Hebrew University of Jerusalem, Rehovot 76100, Israel
Abstract
During recent decades there is a significant improvement in the genetic selection for growth rate of broilers coincided with dramatic increase in metabolic rate. However, this selection lacks in comparable development of visceral systems, causing inferior thermotolerance response in broilers. The situation, where growth rate (heat production) improves on a yearly basis and the future foresees increase in global surface temperature, demands an efficient means to economically improve the acquisition of thermotolerance by broiler chickens exposed to hot climatic conditions. To develop thermotolerance three direct responses are employed by the broiler: the rapid thermal shock response, acclimation/acclimatization, and epigenetic adaptation. The last one has been successfully modulated by early-age thermal manipulations of postnatal chicks. However, uniform post-hatch temperature manipulation is difficult to adopt, whereas the use of such manipulations during incubation would probably be more efficient and uniform. alteration of the energy balance set point.
The hypotheses underlying these studies are: a. during embryogenesis, it is possible to induce long-lasting physiological memory, based on epigenetic adaptation; b. thermal manipulations have to be induced during sensitive periods, by means of a specific level and duration of heat exposure. Heat thermal manipulations (TM - 39.5oC; 65% RH continuously or for 12 hours/day) during the period of the hypothalamus-pituitary-thyroid or adrenal axes development and maturation (embryonic days 7 to 16), demonstrated a significant improvement of thermotolerance acquisition in broilers up to marketing age. This improvement was tested by acute heat exposure, and was characterized by a significant reduction of heat production, coincided with significant increase in sensible heat loss by radiation and convection, and significant decline in the broiler stress level. Furthermore, the treated chickens exhibited significantly higher relative breast muscle weight and significantly lower abdominal fat pad weight. It can be concluded that a long-lasting effect of embryonic TM on the thermoregulatory abilities of the chicken is applicable. This long-lasting thermal memory is probably a result of epigenetic temperature adaptation, which is characterized by an alteration of the energy balance set point.Keywords: broilers; thermal manipulation (TM); embryogenesis; thermoregulation; epigenetics.
Introduction
In endothermic animals (mammals and birds) body temperature (Tb) is the most physiologically guarded parameter of the body. Therefore, the thermoregulatory system in these animals operates at a very high gain, in order to control Tb within a relatively narrow range, despite moderate to extreme changes in the environmental conditions. The ability to maintain a stable Tb springs from the mechanisms that control heat production and heat loss; mechanisms that changed in the course of evolution, to enable endothermia instead of ectothermia. The evolutionary changes from endothermia to ectothermia were achieved because the developmental regulatory mechanisms maintained a balance between heat production and heat loss. Both mechanisms, especially heat production, are probably ancient than endothermy, but both are permanently activated and regulated by either/both neuronal and hormonal signals (Silva, 2006; Morrison et al., 2008; Richards and Proszkowiec-Weglarz, 2008).
Recent decades have seen significant development in the genetic selection of the meat-type fowl, i.e., broilers (Havenstein et al., 2003a), which has led to rapid growth, accompanied by increased feed efficiency and metabolic rate which provides the poultry industry with heavy domestic fowl in relatively short growth periods. Such development logically necessitates parallel increases in the size of the cardiovascular and respiratory systems, as well as enhancements in their functional efficiency. However, inferior development of such major systems (Havenstein et al., 2003b) has led to relatively low capability to balance energy expenditure and body water balance under extreme environmental conditions. Thus, acute exposure of chickens to extreme conditions (hot spells) has resulted in major economic losses. During the late 19th and the 20th centuries the global mean surface temperature increased by 0.8-1.7°C (U.S. National Climatic Center, 2001), and scientists expect that there will be a further increase of 0.6-2.5°C during the next 50 years. This situation, in which growth rate improves annually, accompanied by increased heat production, and future increases in global surface temperatures are foreseen, demands an efficient and economical means to improve the acquisition of thermotolerance by domestic fowl exposed to hot climates.
Birds are homeotherms enable to maintain their body temperature (Tb) within a narrow range. However, an increase in body temperature above the regulated range, as a result of exposure to environmental conditions and/or excessive metabolic heat production, may lead to a cascade of irreversible thermoregulatory events that could be lethal for the bird. To sustain thermal tolerance and avoid the deleterious consequences of thermal stresses, three direct responses are elicited (Yahav, 2009): the rapid thermal stress response-RTSR characterized by minutes to hours response, acclimation/acclimatization characterized by days to weeks response (Yahav et al., 1997a), and embryonic or post-hatch thermal manipulation (TM), based on epigenetic adaptation during the perinatal period and based on timing (Tzschentke et al., 2004). Acclimation might serve as an efficient tool to improve the acquisition of thermotolerance. However, the process of acclimation, at least in broilers, is rendered rather impracticable by the early marketing age of broilers, coupled with: (a) the necessity to keep the environmental temperature controlled up to the age of 21 d for brooding; (b) the deleterious effect of acclimation on broiler performance; and (c) the enormous cost of temperature-controlled poultry houses. The limitations outlined above have led to the investigations of how to adopt epigenetic adaptation efficiently in broilers.
The incubation period of broilers gets more attention during the last decade. It can be related to the recognition that during this period various environmental manipulations may induce long-lasting-physiological-memory caused by epigenetic adaptation.
Epigenetic adaptation, which has been defined as a lifelong adaptation that occurs during prenatal (embryogenesis) or early post-hatching ontogeny, takes place within critical developmental phases that affect gene expression (Nichelmann and Tzschentke, 2002; Tzschentke and Plagemann, 2006) and seems to be a suitable means of reaching the goal of improved acquisition of thermotolerance in broilers (Yahav et al., 2009) or affecting the cardiovascular system (Zoer et al., 2009). During early development most functional systems evolve from an open-loop system without feedback to a closed control system with feedback (“transformation rule”) (Dörner, 1974). Environmental manipulations during the critical phases of development process may induce alterations in the control systems.
The hypotheses underlying studies related to epigenetic adaptation are that: 1. during embryogenesis, it is possible to induce long-lasting physiological memory, based on epigenetic adaptation; 2. long-lasting memory can be defined, most probably, as alteration in the control systems threshold response to changes in the environment; and 3. environmental manipulations by means of specific levels and durations of exposure, during sensitive periods within embryogenesis will impart improved the broiler's response during the entire life span.
In contrast to the uniform environmental conditions of commercial incubation, in nature, incubation conditions are non-uniform, because of the need to search for food and escape from predators, because of non-uniform nest insulation (Webb, 1987) and because of different nesting altitude. This may be one of the reasons why birds in the wild are quite capable of coping with extreme environmental temperatures.
The chicken (Gallus gallus) embryo represents an excellent model for investigating developmental physiology of the thermoregulatory (Piestun et al., 2008) and of the cardiovascular system (Ruijtenbeek et al., 2002). Since the embryo develops outside the mother, effects of external stressors on thermoregulation and cardiovascular development can be studied independently of any confounding influences from alterations in maternal hormonal, metabolic, or haemodynamic status. However, there is still one main dilemma underlying the environmental manipulations during incubation which is how to sustain the embryo development, hatchability and growth performance post-hatch despite the manipulations. For example, it is well known that development in chronic hypoxia produces significant abnormalities in the developing cardiovascular system, as well as increased mortality and decreased body weight (Villamor et al. 2004).
This paper will focus on TM during embryogenesis and their effects on thermotolerance acquisition and performance of broiler chickens.
Hot manipulations during incubation
In recent experiments (Piestun et al., 2008) TM at 39.5°C and 65% RH was applied continuously (24H treatment) or intermittently for 12 h per day (12H) to broiler embryos from days E7 to E16 (inclusive). After hatching, chicks were raised under standard conditions to 35 d of age and then subjected to thermal challenge (35°C for 4.0 h).
Figure 1: The effect of thermal manipulation of 39.5°C and 65% relative humidity for 12 hours/day (12H) or continuously (24H) from 7 days of incubation (E7) to E16 (inclusive), on egg shell temperature during incubation. Embryo's heat production symbolizes the time when embryos metabolic rate increases to a level allowing Tegg higher than incubation temperature. In each embryogenesis day, values designated by different letters differ significantly (P≤0.05). (According to Yahav et al., 2009).
uring incubation, only the 24H treatment negatively affected embryo growth and development, with lower relative weights of embryo, liver and pipping muscle. During TM (Piestun et al., 2009), egg shell temperature (Figure 1), heart rate and oxygen consumption were elevated as embryos were in their ectothermic phase, but from the end of the TM until hatch these parameters were significantly lower in both treatments than in the control. Moreover, plasma concentrations of the thyroid hormones were significantly lower in the two treatments during and after TM, until hatch. Plasma corticosterone concentration of the TM-treated embryos was significantly lower after the TM but significantly higher at hatch. These results let to the conclusions that TM during the development of the thyroid and adrenal axis lowered their functional set point, thus lowering metabolic rate during embryogenesis and at hatch.
Figure 2: The effects of TM applied continuously (24H) or intermittently for 12h/d (12H) from 7 to 16 d of incubation (inclusive) on the profile of hatching (according to Piestun et al., 2008).
A significant decline in hatchability was recorded in the 24H TM broiler eggs (Figure 2). This was mainly because of embryos that initiated external piping but were not able to complete it, most probably as a result of insufficient accumulation of glycogen in the liver and the Musculus complexus (Christensen et al., 2001). The hatched chicks of the 24H TM treatment were further characterized by lower chick quality and significantly lower body weight. However, the 12H treatment did not significantly affect hatchability or chick quality (Piestun et al., 2008).
Application of TM, either continuously in treatment 24H or intermittently in treatment 12H, caused a significant decline in the metabolic rate of the hatched chicks, emphasizing the significant effect of TM in reducing the metabolic rate. This was manifested in a significantly reduced Tb, accompanied by significantly reduced plasma T4 and T3 concentrations (Piestun et al., 2008). Although T3 is the most potent hormone with regard to the chick’s metabolic rate, the fact that plasma T4 concentration was also significantly reduced in the hatched TM chicks suggests that the activity of the thyroid gland was reduced upon hatch.
Piestun et al. (2008) had demonstrated for the first time that adopting E7 to E16 as the “critical phase” for TM of chick embryos significantly enhanced thermotolerance. In this study, Tb of the treated chickens remained significantly lower throughout the growth period of 35 days, suggesting that the metabolic rate was lower.
Figure 3: The effects of TM applied continuously (24H) or intermittently for 12h/d (12H) from 7 to 16 d of incubation (inclusive) on plasma corticosterone concentrations of 35-d-old male broiler chickens that had not experienced thermal challenge at this age (naïve), or were acutely exposed to 35°C for 2.5 h (challenged) (according to Piestun et al., 2008).
Moreover, thermal challenge of 35-d-old broilers at 35°C for 4 h resulted in a significant improvement in the acquisition of thermotolerance in both the 12H and 24H TM treatments; an improvement that was characterized by a significant lower level of stress, as indicated by the level of plasma corticosterone (Figure 3), and by a mortality rate half that of the control chickens. However, whereas in the 24H treated broilers deleterious effects on performance were demonstrated, the 12H broilers were not affected by TM during incubation. Furthermore, the manipulated broilers exhibited a significant heavier breast muscle relative weight, coupled with lower to significant lower relative weight of abdominal fat pad.
This accumulating evidence shows that the epigenetic adaptation approach, and its association with changes in the incubation environment, with emphasis on fine-tuning the level and duration of stress to coincide with the “critical phase,” can elicit the improvement of thermotolerance acquisition and the high and sustainable performance.
Acknowledgements
This research was supported by research grant No. IS-3836-06R from BARD, the United States – Israel Binational Agricultural Research and Development Fund, and by grant No. 356-0416 from the Egg and Poultry Board of Israel.