Feeding the early gestating gilt during heat stress

What are the implications towards fetal viability, growth and development?

By MaryKate H. Byrd and Jay S. JohnsonGestational heat stress has a multitude of short and long-term negative effects on the sow and her developing fetuses¹. It has direct effects on sow reproductive success such as reductions in the number of liveborn and an increase in post-weaning return to estrus. Additionally, gestational heat stress can have downstream negative impacts on piglet growth, stress response and immune function during postnatal life. Efforts by our group have sought to prevent these negative effects from impacting the profitability and sustainability of the swine industry. However, to achieve this goal, it is necessary to characterize and identify mechanisms by which gestational heat stress impacts sow health and fetal development. Therefore, we sought to better understand how early gestational heat stress influences fetal development and viability, and whether maternal feed energy partitioning plays a role. Eleven pregnant gilts were exposed to gestational thermoneutral conditions (18.5 ± 1.2°C; 60.9 ± 15.2% relative humidity), and 12 pregnant gilts were exposed to gestational heat stress conditions (cyclic 26 to 36°C; 54.2 ± 18.5% relative humidity) from day 6 to 33 of gestation. Gilts were limit-fed and consumed the same amount of feed (1.82 kg per day) regardless of the environment they were housed in. Water was provided ad libitum. Body temperature was recorded every 15 minutes throughout the study and body weights were recorded weekly. On day 33 of gestation, the gilts were harvested, and the reproductive tract and fetuses were collected. The whole tract weight, corpus lutea counts, the number of fetuses per horn, and individual fetal weights were recorded. Fetal images were taken to measure individual fetal length, width, and crown rump length. Fetuses were classified as non-viable by abnormal physiological development or if crown rump length was two standard deviations below the litter average.Gilts exposed to gestational heat stress conditions had increased internal body temperature when compared to gilts exposed to gestational thermoneutral conditions (Fig. 1A). This confirmed that the environmental treatment protocol caused heat stress in the gestating gilts. Despite this, the heat stressed gilts had a greater average daily gain (Fig. 1B) and were more feed-efficient than their thermoneutral counterparts (Fig. 1C). Additionally, the efficiency of converting feed energy into body mass was improved for heat stressed gilts when compared to thermoneutral gilts (Fig. 1D). Taken together, these results indicate that the heat stressed gilts were in a more positive energy balance when compared to thermoneutral gilts, despite being at the same plane of nutrition as indicated by similar feed intake. Although heat stressed gilts were in a more positive energy balance, no subsequent improvement in fetal growth or reproductive tract size was observed (Table 1). This indicates that excess energy availability for the heat stressed gilts was not partitioned towards reproduction but was retained by the gilt, possibly as adipose tissue. A recent study by our group (unpublished data) confirmed this hypothesis and demonstrated that heat stressed gestating gilts had a greater increase in backfat when compared to thermoneutral controls (Fig. 2). Similar to previously published research^2-4, early gestation heat stress negatively influenced fetal counts. Independent of ovulation rate, the ratio of total fetuses (Fig. 3) and viable fetuses (Fig. 4) to corpus lutea were reduced in heat stressed versus thermoneutral gilts. These measures imply that early fetal losses were greater in heat stressed versus thermoneutral gilts (Fig. 5), which would likely result in a decrease in litter size. However, no morphological differences were observed (Table 1).A central tenet of heat stress biology is that exposure to temperatures above an animal's upper critical temperature results in greater maintenance costs due to energy requirements for thermoregulation and increased chemical reaction rates in the body⁵. Increased maintenance costs have been reported in several livestock species, including cattle⁶ , lambs⁷ and pigs⁸. Given these reports, when considering the partitioning of net energy into either maintenance costs or growth (Fig. 6), it is logical to infer that maintaining heat-stressed pigs at the same plane of nutrition as thermoneutral pigs would result in decreased growth for the former. However, results from the present study and others⁹ demonstrate that heat stress exposure at the same nutritional plane causes pigs to grow at a faster rate. The most likely explanation for this response is that the level of heat stress used in this study and others⁹ results in an overall decrease in maintenance costs for pigs. This hypothesis has been experimentally confirmed by our group^{10, 11}, and others^12,13and may be due to either a decrease in visceral mass or a reduced requirement to produce metabolic heat to maintain body temperature. Regardless of the reason for the improved growth rate and feed efficiency of heat-stressed pregnant gilts in the present study, it appears that the increase in available net energy for growth was not partitioned towards the developing reproductive tract or fetuses during early gestation. Implications from this study are that the practice of feeding gestating gilts (and possibly sows) to maintenance may differ based on environmental conditions. For example, it was determined that heat-stressed gestating gilts required only 64% of the total net energy intake to gain similar weight as the thermoneutral gestating gilts. However, more research should be conducted to confirm these results under varying heat stress conditions and to better understand the economic implications.References
[1] Johnson, J.S., Stewart, K.R., Safranski, T.J., Ross, J.W., and Baumgard, L.H. 2020. In utero heat stress alters postnatal phenotypes in swine. Theriogenology. 154: 110-119. Doi:10.1016/j.theriogenology.2020.05.013.[2] Tompkins E.C., Heindenreich, C.J., and Stob, M. 1967. Effect of post-breeding thermal stress on embryonic mortality in swine. J. Anim. Sci. 26:377-380. Doi:10.2527/jas1967.262377 [3] Omtvedt, I.T., Nelson, R.E., Edwards, R.L., Stephens, D.F., and Turman, E.J. 1971. Influence of heat stress during early, mid and late pregnancy of gilts. J. Anim.Sci.32:312-318. Doi: 10.2527/jas1971.322312x.[4] Edwards, R.L., Omtvedt, R.L., Turman, E.J., Stephens, D.F., and Mahoney, G.W.A. 1968. Reproductive performance of gilts following heat stress prior to breeding and in early gestation. J. Anim. Sci. 27:1634-1637. oi:10.2527/jas1968.2761634x [5] Kleiber, M. 1961. The fire of life: An introduction to animal energetics. John Wiley & Sons, New York, NY, and London, UK. p. 146-174.[6] Beede, D.K., and Collier, R.J. 1986. Potential nutritional strategies for intensively managed cattle during thermal stress. J. Anim. Sci. 62:543–554. Doi:10.2527/jas1986.622543x[7] Ames, D.R., and Brink, D.R. 1977. Effect of temperature on lamb performance and protein efficiency ratio. J. Anim. Sci. 44:136–144. Doi:10.2527/jas1977.441136x[8] Campos, P. H., Noblet, J., Jaguelin-Peyraud, Y., Gilbert, H., Mormede, P., de Oliveira Donzele, R.F.M., Donzele, J.L., and Renaudeau, D. 2014. Thermoregulatory responses during thermal acclimation in pigs divergently selected for residual feed intake. Int. J. Biometeorol.58:1545–1557. [9] Pearce, S. C., Gabler, N.K., Ross, J.W., Escobar, J., Patience, J.F., Rhoads, R.P., and Baumgard, L.H. 2013. The effects of heat stress and plane of nutrition on metabolism in growing pigs. J. Anim. Sci. 91:2108–2118. Doi: 10.2527/jas.20125738[10] Johnson, J.S., Sanz-Fernandez, M.V., Gutierrez, N.A., Patience, J.F., Ross, J.W., Gabler, N.K., Lucy, M.C., Safranski, T.J., Rhoads, R.P., and Baumgard, L.H. 2015. Effects of in utero heat stress on postnatal body composition in pigs: I. Growing phase. J. Anim. Sci. 93: 71-81. Doi: 10.2527/jas.2014-8354.[11] Johnson, J.S., Sanz-Fernandez, M.V., Patience, J.F., Ross, J.W., Gabler, N.K., Lucy, M.C., Safranski, T.J., Rhoads, R.P., Dubois, S., and Noblet, J. 2001. Effect of high temperature on feeding behavior and heat production in group-housed young pigs. Br. J. Nutr. 86:63–70. Doi: 10.1079/BJN2001356[12] Collin, A., van Milgen, J., Dubois, S., and Noblet. J.. 2001. Effect of high temperature on feeding behavior and heat production in group-housed young pigs. Br. J. Nutr. 86:63–70. Doi: 10.1079/BJN2001356[13] Renaudeau, D., Frances, G., Dubois, S., Gilbert, H., and Noblet, J. 2013. Effect of thermal heat stress on energy utilization in two lines of pigs divergently selected for residual feed intake. J. Anim. Sci. 91:1162–1175. Doi: 10.2527/jas.2012-5689

Figure 1. Effects of heat stress (cyclic 26 to 36°C; 54.22 ± 18.46% relative humidity) or thermoneutral (18.5 ± 1.2°C; 60.9 ± 15.2% relative humidity) conditions on the (A) Vaginal temperature, (B) average daily gain (ADG), (C) feed efficiency (gain : feed), and (D) ADG : Net energy (NE) intake of gestating gilts.

Figure 2: Change in backfat in gestating gilts exposed to heat stress (cyclic 26 to 36°C; 54.2 ± 18.5% relative humidity) or thermoneutral (18.5 ± 1.2°C; 60.9 ± 15.2% relative humidity) conditions from d 6 to 60 of gestation (unpublished data).

Figure 3: Total fetuses : CL of gestating gilts exposed to heat stress (cyclic 26 to 36°C; 54.2 ± 18.5% relative humidity) or thermoneutral (18.5 ± 1.2°C; 60.9 ± 15.2% relative humidity) conditions.

Figure 4. Viable fetuses : CL of gestating gilts exposed to heat stress (cyclic 26 to 36°C; 54.2 ± 18.5% relative humidity) or thermoneutral (18.5 ± 1.2°C; 60.9 ± 15.2% relative humidity) conditions.

Figure 5. Total fetuses subtracted from total CL (CL - Fetuses) in gestating gilts exposed to heat stress (cyclic 26 to 36°C; 54.2 ± 18.5% relative humidity) or thermoneutral (18.5 ± 1.2°C; 60.9 ± 15.2% relative humidity) conditions.

Figure 6. Energy partitioning from gross energy in feed to net energy for maintenance and growth.

Byrd is a PhD candidate and graduate research assistant and Johnson is supervisory research animal scientist at the USDA-ARS Livestock Behavior Research Unit, both at Purdue University.