Effect of temperature and humidity on reproductive performance of crossbred sows in Thailand

Theriogenology 65 (2006) 606–628 www.journals.elsevierhealth.com/periodicals/the

Effect of temperature and humidity on reproductive performance of crossbred sows in Thailand Annop Suriyasomboon a,c,e, Nils Lundeheim b,e, Annop Kunavongkrit d, Stig Einarsson a,e,* a

Department of Clinical Sciences, Faculty of Veterinary Medicine and Animal Sciences, Swedish University of Agricultural Sciences, P.O. Box 7054, SE-75007 Uppsala, Sweden b Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, SE-75007 Uppsala, Sweden c Department of Animal Husbandry, Chulalongkorn University, 10330 Bangkok, Thailand d Department of Obstetrics, Gynaecology and Reproduction, Chulalongkorn University, 10330 Bangkok, Thailand e Centre for Reproductive Biology in Uppsala, Uppsala, Sweden Received 18 April 2005; received in revised form 3 June 2005; accepted 6 June 2005

Abstract This study investigated the influence of season, temperature, and humidity on the reproductive performance of sows under tropical conditions. Data were collected from 11 sow herds from January 2001 to June 2002. Temperature and humidity were recorded daily for each herd from January 2001 to February 2002. Semen used was collected from boars housed in conventional open-air stables (six herds) or in evaporative cooling stables (five herds). A total of 43,875 farrowing records were included in the statistical analysis. Fourteen-day moving averages of daily maximum temperature and minimum humidity were calculated and merged with each reproductive record. ANOVA was applied to the reproductive records. In addition to the fixed effects included in the statistical models (e.g. system, season, parity, temperature, and humidity), the random effect of herd within system was included. The total number of piglets born was analyzed in relation to the climate at previous weaning (NTB-w), at mating (NTB-m), and at farrowing (NTB-f). The housing system of the boars had no significant effect on any of the reproductive variables analyzed. Season (2-month periods) as well as parity number had a significant effect on all reproductive variables analyzed. Increased length of previous lactation had a significant and favorable effect (P < 0.001) on NTB-w, NTB-m, and weaning-to-first-service interval. There were indications that high temperature and humidity * Corresponding author. Tel.: +46 18 672170; fax: +46 18 673545. E-mail address: [email protected] (S. Einarsson). 0093-691X/$ – see front matter # 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.theriogenology.2005.06.005

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

607

(recorded at the herd level) at previous weaning/mating or at farrowing had negative effects on litter size, but these negative influences were not consistent. # 2005 Elsevier Inc. All rights reserved. Keywords: Sow; Season; Temperature; Humidity; Reproductive performance

1. Introduction It is well established that reproductive efficiency in sows depends on several factors, such as parity number, breed, season, temperature, photoperiod, and nutrition [1–12]. Season is regarded as an important environmental factor causing variation in sow fertility. Several studies have shown that the adverse effects of high ambient temperature, humidity, and/or changes in photoperiod, are characterized by a decreased farrowing rate, prolonged weaning-to-first-service interval, and in some cases, decreased litter size during some part of the year [1–12]. High ambient temperature leading to heat stress has been associated with seasonal infertility. This is especially true not only in tropical areas, for example, in Thailand, where the temperature exceeds 30 8C for several months of the year [10,13], but also in temperate areas, for example, in countries in northern Europe and the USA [6,11,12]. Several experimental studies have been performed using two or more temperature levels kept constant over the day at a low or moderate relative humidity [7,8,14–20]. Little information is available as to the combined effects of high humidity and variable day temperature. Most relevant field studies are based on general climatic data obtained from meteorological stations. To our knowledge, no study of the direct effects of temperature and humidity on the reproductive performance of sows, in which daily climatic data were collected within the herd, has been performed under tropical conditions with high ambient temperature and humidity. In Thailand, most pigs are raised in conventional open-air stables (CONV) where ambient temperature, relative humidity, and photoperiod follow those of the outside. The evaporative cooling (EVAP) housing system has been introduced to improve the microclimate for farm animals in Thailand, and is being used for the boars of several sow herds. The EVAP system aims to reduce the temperature via a humidification process. In EVAP, water is sprayed onto cooling pads at one end of a closed stable. Hot outdoor air is drawn through the pads by exhaust fans at the other end of the building, and the temperature is lowered as the water evaporates. This process reduces the temperature while increasing the relative humidity in the air [21]. This study investigated the effects of season, temperature, humidity, parity number, and lactation length on the reproductive performance of crossbred sows under tropical conditions in Thailand, where the boars were kept either in CONV or EVAP housing.

2. Materials and methods This study is based on data pertaining to 11 sow herds located in central Thailand. Six of these herds had CONV housing while five herds used EVAP housing system for their boars.

608

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

Table 1 Characteristics of the herds included in this study Herd

1 2 3 4 5 6 7 8 9 10 11

System of boar housing EVAP EVAP EVAP EVAP EVAP CONV CONV CONV CONV CONV CONV

a

Year of installation of EVAP system for boars 1998 1999 1999 1998 1997

Herd size Total number of sowsa

Total number of boars

4900 4000 1100 1900 5200 4300 1900 1500 600 1800 900

85 135 20 25 40 40 35 35 20 95 20

Number of farrowing units

Herd-monitoring program

5 7 1 1 8 8 5 5 1 5 1

PigLIVE1 PigLIVE1 PigCHAMP1 PigCHAMP1 Smilepig1 Smilepig PigLIVE1 PigLIVE1 PigLIVE1 PigLIVE1 PigLIVE1

CONV CONV EVAP; 1 CONV EVAP; 3 CONV CONV CONV CONV CONV CONV CONV CONV

Gilts not included.

Each herd had only one of the housing systems for boars. All herds had been in production for at least 10 years, and the herds with EVAP housing for the boars had used this system for at least 1 year before the start of the study. The available data include mating and farrowing records for the January 2001 to June 2002 period. Crossbred sows (Landrace  Yorkshire) and Duroc boars were present in all herds. The first author of this article visited the herds every 2 weeks to monitor their health and check the integrity of the data gathered by the PC-based herd-monitoring programs. Incorrect data were corrected when possible. The herds are described in Table 1. 2.1. Herd management The sows were kept in individual stalls in a conventional open-air stable during gestation, while lactating sows were kept in individual farrowing pens. In two of the herds with EVAP housing for the boars, some of the lactating sows were also kept in EVAP stables. In the CONV housing, cooling systems such as water sprinkling, fogging, and fans were turned on when the sows seemed to feel uncomfortable due to high temperature. The sow feed contained approximately 17% crude protein and 3100 kcal of digestible energy per kilogram (kg). Feed ingredients included broken rice, rice bran, soybean meal, fishmeal, dicalcium phosphate, salt, vitamins, and mineral concentrate. All sows received feed of the same composition at all stages of the reproductive cycle. Antibiotics were added to the sow feed when needed to control mastitis, metritis, agalactia, and dysentery. Sows were fed 1.8 kg feed/day from mating to 12 week of gestation, and thereafter 3 kg feed/day until 7 days before expected farrowing, when the feed amount was reduced to 2 kg feed/day. Lactating sows were fed 2.5, 4.5, and 6 kg feed/ day during weeks 1, 2, and 3–4 of lactation, respectively. After weaning, the sows were moved to the mating/gestating area, and until mating were fed 3 kg feed/day. All gestating and lactating sows had free access to water via nipples.

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

609

Replacement gilts were penned in groups of 3–5. Before expected estrus, they were moved into the mating area for boar contact, where they were kept in individual stalls. Estrus detection of gilts and sows was performed twice a day, in the morning and evening, by experienced staff in the presence of boar(s). If onset of standing heat was detected in the morning, the sows were mated in the evening; if onset of standing heat was detected in the evening, the sows were mated in the morning. Most matings were performed by AI, and the AI doses were produced in each herd. Matings were immediately recorded on both sow cards and mating reports, to be entered into the computer. After mating, backpressure testing in the presence of a boar (control of repeat breeding) was performed from the second through third week after mating. Five weeks after mating, pregnancy was tested by A-mode ultrasound. Farrowing was supervised during working hours (06:00–18:00 h), and farrowing events were recorded twice a day. All the live-born piglets were weighed together, and their total weight was recorded. Cross fostering was performed within a few days of farrowing. Creep feed was provided from day 7 after farrowing. The average lactation period, across all 11 herds, was approximately 24 days (98.7% within the 16–35-day range). Weaning was done twice a week; at weaning, sows were moved to the mating area and penned in individual stalls adjacent to the boar(s). Sows that did not show estrus within 7 days were stimulated to come into estrus by relocation to another individual stall, or sometimes by a combination of relocation and grouping of three to four sows together, and introducing them into the boar pen for 10 min twice a day. The sows that had not shown estrus by the end of the second week after weaning were treated with hormones (PG6001; Intervet, The Netherlands). In the herds studied, there were no clinical findings of foot-and-mouth disease or swine fever during the period studied. Antibodies against porcine reproductive and respiratory syndrome (PRRS) were found, but no clinical outbreak was observed. Culling due to small litter size was done in the first to third parities, and due to conception failure after the third remating. Culling due to old age was planned for after parity 8. 2.2. Temperature and humidity Temperature and humidity were recorded once a day, using a digital max–min thermohygrometer (Biltema, Sweden), in one conventional farrowing stable in each of the 11 herds in January 2001 to February 2002 period. The device was placed in the middle of the stable hanging from a hook 1.2–1.5 m above the floor. Temperature and humidity were recorded every day around 15:00–16:00 h and after each recording the device was reset to measure new figures for the next day. The daily records included maximum, minimum, and current actual figure for both temperature (8C) and humidity (% relative humidity, % RH). In most tropical areas, including in Thailand, day length is nearly uniform, being approximately 12  1 h, throughout the year. In Thailand, there are three seasons: the hot season from March to June, rainy season from July to October, and winter season from November to February. In one herd representing each type of system, temperature and humidity were measured every hour for 10 days for each of these three seasons, using

610

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

HOBO1 H08 data loggers (Onset Computer Corporation, MA, USA, www.onsetcomp.com). This information is presented elsewhere [22]. 2.3. Definitions Weaning-to-first-service interval (WSI) is defined as the number of days from weaning to the first service within 30 days after weaning. The day of weaning is defined as day 0, and WSI longer than 30 days is regarded as a missing value. Service within 7 days after weaning (WSI7) and remating (RR) are binomial traits, defined for the first matings in the 0–30-day interval after weaning. WSI7 is defined as 1 for matings 0–7 days after weaning, and as 0 for matings 8–30 days after weaning. RR is defined as 1 for rematings taking place 18–100 days after the first mating, and as 0 if no remating was recorded 18–100 days after the first mating. 2.4. Data editing Data were extracted from three herd-monitoring PC programs – PigCHAMP1 (Version 4.0, Farms.com Ltd.; two herds), PigLIVE1 (Version 2.0, Live Informatics Co. Ltd., Thailand; seven herds), or Smilepig1 (Version 1.53, Laemthong Corporation Co. Ltd., Thailand; two herds) – and handled using the SAS program (Version 8, SAS Institute Inc., Cary, NC, USA). The captured records covered sow identity, breed, parity number, mating date, farrowing date, total number of piglets born per litter (NTB), number of piglets born alive per litter (NBA), number of stillborn piglets per litter (NSB), average piglet birth weight (AVBWT), weaning date, and number of weaned piglets per litter. Variables such as lactation length (LL), gestation length, WSI, WSI7, and RR were calculated from the data (see definitions above). Obviously incorrect recordings were treated as missing values in the statistical analysis. Some records were systematically excluded: records from purebred sows and breed combinations other than Landrace  Yorkshire, farrowing records when previous parity and/or present parity took place in an EVAP stable (two of the herds), and records from parities higher than 8. LL values shorter than 16 days or longer than 35 days, WSI values longer than 30 days, and AVBWT values less than 0.5 or higher than 2.5 kg were treated as missing values in the statistical analysis. No limitation due to extreme values of NTB, NBA, and NSB was applied. For the statistical analysis, parity was grouped into five classes: 1, 2, 3, 4–5, and 6–8. Lactation length (LL) was grouped into four classes: 16–21, 22–23, 24–26, and 27–35 days. Two-month farrowing, weaning, and mating periods were constructed: January/ February, March/April, May/June, July/August, September/October, and November/ December. Fourteen-day moving averages of daily maximum temperature and daily minimum humidity in the farrowing stables were calculated for each herd and day. Reproductive records were merged with their corresponding moving averages 14 days before weaning, 14 days after the first mating after weaning, and 14 days before farrowing. If the moving average was based on data from less than 13 days, the moving average was blanked. The moving averages of daily maximum temperature (T) and daily minimum humidity (H) were grouped into three classes to obtain approximately equal numbers of

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

611

observations in each class: for T = truncation points 33.1 and 35.1 8C; for H = truncation points 45 and 51% RH. NTB was analyzed in relation to the climate at weaning (NTB-w, litter size in next parity), at the first mating after weaning (NTB-m, litter size in next parity), and at farrowing (NTB-f). As a consequence, litter size in the first parity was only included in NTB-f. Litters resulting from remating were excluded when analyzing NTB-w and NTB-m. The statistical analysis was restricted to events taking place in the January 2001 to February 2002 period. However, data was also captured from the March 2002 to June 2002 period for analyzing NTB-w, NTB-m, and RR. After exclusions, data comprised 43,875 records. There were 38,495 complete farrowing records with information on both T and H for the 14 days before farrowing. The corresponding number of complete records with information on both T and H for the 14 days before weaning and the 14 days after the first mating were 37,346 and 37,340, respectively. Frequency analysis of the remating pattern of the first remating (regular return: repeat mating within 18–24 days or 39–45 days; irregular return: repeat mating within 25–38 days or 46–100 days after the first mating), was based on 4324 remating records where the first mating took place in the January 2001 to February 2002 period. 2.5. Statistical analysis Data were statistically analyzed using the SAS program (Version 8, SAS Institute Inc., Cary, NC, USA). Analysis of variance was performed using PROC MIXED for NTB-f, NTB-w, NTB-m, NBA, NSB, AVBWT, and WSI, and the GLIMMIX Macro for the categorical traits WSI7 and RR. For analyzing the seasonal variation (Table 3a), the statistical models included the fixed effects of housing system for boars (system), 2-month periods (farrowing month for NTB-f, NBA, NSB, and AVBWT; weaning month for WSI, WSI7, and NTB-w; and the first service month for RR and NTB-m), parity, and the interaction between system and 2-month periods (for NTB-w, NTB-m, and RR, but not for the variables for which this interaction was not supposed to cause any variation, such as WSI and WSI7), and between parity and 2-month periods. The effects of temperature and humidity in the 14 days before farrowing (NTB-f, NBA, NSB, and AVBWT), 14 days before weaning (WSI, WSI7, and NTB-w), and 14 days after the first service after weaning (RR and NTB-m) were analyzed. The fixed effects of system, parity, T, H, and the interactions between system and T as well as between system and H (for NTB-w, NTB-m, and RR; see above), between parity and T, between parity and H, and between T and H were included in the statistical model (Table 3b). LL (previous parity) was also included in the statistical model when analyzing NTB-w, NTB-m, WSI, WSI7, and RR. A regression on NTB-f was included in the statistical model when analyzing AVBWT. The random effect of herd within system was included in all statistical models. Multiple comparison testing of leastsquares means (LSmeans) was performed using Bonferroni correction, to reduce the risk of obtaining false significances. Chi-square analysis (PROC FREQ) was used to analyze the frequency distribution of regular/irregular return in relation to parity and season. Levels of significance are given conventionally: ns = no significant difference (P > 0.05); and significant difference * 0.01 < P  0.05, **0.001 < P  0.01, ***P < 0.001.

612

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

3. Results Descriptive statistics of the data after editing are shown in Table 2. The mean parity number after exclusion of parities greater than 8 was 3.6 in the CONV system and 3.7 in the EVAP system. The means of NTB, NBA, NSB, AVBWT, WSI, WSI7, and RR were approximately the same in both systems: 10.5 piglets, 9.9 piglets, 0.7 piglets, 1.6 kg, 5.9 days, and 88.3 and 9.6%, respectively, in the CONV system; 10.5 piglets, 9.8 piglets, 0.7 piglets, 1.5 kg, 6 days, and 88.8, and 10.9%, respectively, in the EVAP system. The mean gestation and lactation lengths as well as the moving averages of daily maximum temperature and daily minimum humidity were approximately the same in both systems: 115 and 24 days, and 33.9 8C and 50% RH, respectively. The levels of significance of all fixed effects included in the statistical models are presented in Table 3a (effect of season) and Table 3b (effect of temperature and humidity). System was found to have no significant effect on any of the reproductive variables Table 2 Descriptive statistics of the data after editing System

N

Mean

S.D.

Range

Parity number

CONV EVAP

17110 26765

3.6 3.7

2.1 2.1

1–8 1–8

Gestation length (days)

CONV EVAP

17085 26748

115.3 115.1

1.7 1.8

107–122 107–122

Total number of piglets born per litter

CONV EVAP

17110 26765

10.5 10.5

2.8 2.7

1–24 1–24

Number of piglets born alive per litter

CONV EVAP

17110 26765

9.9 9.8

2.8 2.5

0–19 0–20

Number of stillborn piglets per litter

CONV EVAP

17110 26765

0.7 0.7

1.2 1.3

0–14 0–19

Average piglet birth weight (kg)

CONV EVAP

16989 26693

1.6 1.5

0.3 0.2

0.5–2.5 0.5–2.5

Lactation length (days)

CONV EVAP

16864 26475

24.7 24.0

2.8 3.8

16–35 16–35

Weaning-to-first-service interval (days)

CONV EVAP

16716 26096

5.9 6.0

4.6 4.2

0–30 0–30

Service within 7 days after weaning (%) a

CONV EVAP

16716 26096

88.3 88.8

– –

– –

Remating (%) b

CONV EVAP

16716 26096

9.6 10.9

– –

– –

Maximum temperature moving average (8C)

CONV EVAP

2337 1893

33.9 33.9

2.5 2.1

26.1–41.1 27.9–39.5

Minimum humidity moving average (% RH)

CONV EVAP

2337 1893

50.1 49.0

10.6 8.6

26.3–82.2 28.2–83.8

a b

Based upon those sows which were served within 30 days after weaning. Based upon first service after weaning.

Table 3a The levels of significance for the fixed effects included in the statistical models (1–3), influence of season Total number of piglets born per litter

Number of piglets born alive per litter

Number of stillborn piglets per litter

Average piglet birth weight

Weaning-tofirst-service

Service within 7 days

Remating

NTB-f

NTB-w

NTB-m

1

2

3

1

1

1

2

2

3

ns

ns

ns

ns

ns

ns

ns

ns

ns

***

***

***

***

***

***

***

***

***

***

***

**

***

***

***

***

**

***

–

***

***

–

–

–

***

***

ns

– ns

***

***

–

–

–

***

ns

– ns

–

*

**

***

ns

–a

ns

Regression on number of total born piglets

–

–

–

–

–

***

–

–

–

Number of observations

43875

28628

28647

43875

43875

286282

42536

42536

42514

System Parity 2-month Lactation length Interaction between System and 2-month Parity and 2-month

Model no. 1: month = month of farrowing; Model no. 2: month = month of weaning; Model no. 3: month = month of mating. ns: P > 0.05; *: P < 0.05; **: P < 0.01; ***: P < 0.001. a This interaction was excluded from this analysis due to no convergence.

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

Fixed effects and interactions

613

614

Table 3b The levels of significance for the fixed effects included in the statistical models (1–3), influence of temperature and humidity Total number of piglets born per litter

Number of piglets born alive per litter

Number of stillborn piglets per litter

Average piglet birth weight

Weaning-tofirst-service

Service within 7 days

Remating

NTB-f

NTB-w

NTB-m

1

2

3

1

1

1

2

2

3

ns

ns

ns

ns

ns

ns

ns

ns

ns

***

***

***

***

***

***

***

***

***

*

***

**

*

***

***

***

***

***

*

*

**

ns

***

***

–

ns –

ns

–

ns –

***

***

ns ns ns

– –

ns

ns

*

*

– –

– –

– –

– –

***

*

**

***

***

***

***

ns

***

ns ns

***

***

ns ns

ns ns ns

ns ns

***

– – ns ns

***

*

*

*

Regression on number of total born piglets

–

–

–

–

–

***

–

–

–

Number of observations

38495

25200

25174

38495

38495

38320

37346

37346

37340

System Parity Temperature (T) Humidity (H) Lactation length Interaction between System and temperature System and humidity Parity and temperature Parity and humidity Temperature and humidity

***

*

Model no. 1, effect of moving average of temperature and humidity before farrowing, Model no. 2, effect of moving average of temperature and humidity before weaning, Model no. 3, effect of moving average of temperature and humidity after mating. ns: P > 0.05; *: P < 0.05; **: P < 0.01; ***: P < 0.001.

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

Fixed effects and interactions

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

615

analyzed. However, the interaction between system and 2-month periods was significant (P < 0.001) for NTB-w, NTB-m, and RR. Parity (P < 0.001) and 2-month periods (P < 0.01) had significant effects on all reproductive variables analyzed. The interaction between parity and 2-month periods had a significant effect on three reproductive variables: NTB-w (P < 0.05), NSB (P < 0.01), and AVBWT (P < 0.001). An increase in previous lactation length resulted in a significant increase (P < 0.001) in NTB-w (litter size in next parity), NTB-m (litter size in next parity), and WSI7, and a decrease (P < 0.001) in WSI (LSmeans: 10.6 piglets, 88.4%, 6.2 days [16–21 days]; 11 piglets, 91.2%, 5.6 days [27–35 days]). There was a significant negative regression of AVBWT (P < 0.001) on NTB-f. An increase in NTB-f of one piglet led to a decrease in AVBWT of 0.03 kg. 3.1. Parity influence (from seasonal analysis) The reproductive performance of the sows in relation to parity number is shown in Fig. 1. Both NTB-f and NBA increased with parity number, reaching their maximum values in parities 4–5, and thereafter decreasing to parities 6–8. NTB-f and NBA increased significantly between parities 1, 2, 3 and 4–5, and decreased significantly in parities 6–8. NSB was lowest in parity 2 and highest in parities 6–8. AVBWT was lowest in parity 1 and reached a plateau in parities 2 and 3; thereafter, it decreased significantly as parity number increased. WSI was significantly longer (P < 0.001) in parity 1 than in higher parities. Moreover, WSI decreased significantly between parities 1 and 2, between parities 2 and 3, and between parities 3 and 6–8. WSI7 increased significantly between parities 1 and 2, between parities 2 and 4–5, and between parities 4–5 and 6–8. RR was highest in parity 1 and decreased significantly between parities 1 and 2, reaching a plateau in parities 2, 3, and 4–5, and decreased significantly in parities 6–8. 3.2. Effect of season Fig. 2 shows the effect of season at farrowing, weaning, and mating on the reproductive performance of sows. The estimated least-squares mean of NTB-f was lower than that of NTB-m in all seasons. This is because the first parities were included in NTB-f but not in NTB-m. NTB-f increased from January/February to March/April, decreased thereafter in May/June, and remained at the same level until January/February. NBA increased from January/February to March/April, decreased thereafter gradually in July/August, after which it increased again in September/October, remaining at the same level until January/ February. Both NTB-f and NBA were highest in the hot season (for sows mated in the winter season), and lowest in the rainy season (for sows mated in the hot season). NTB-m was highest in the winter season (sows were mated in the winter season), and lowest in the first part of the rainy season. NSB was highest when litters were born in the hot season and lowest in the winter season. AVBWT was highest in the rainy season and lowest in the hot season, though the difference, in numerical terms, was slight. Sows weaned in March/April had a significantly shorter WSI (P < 0.001) and higher WSI7 (P < 0.01) than did sows weaned in May/June. Sows weaned from May/June through September/October had a prolonged WSI. RR increased from January/February to May/June and reached a plateau

616

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

Fig. 1. Parity influence on reproductive performance in sows. LSmeans with one letter in common are not significantly different (P > 0.05).

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

617

Fig. 2. Seasonal influence on reproductive performance in sows. LSmeans with one letter in common are not significantly different (P > 0.05). ( ) Hot season; ( ) rainy season; ( ) winter season.

by July/August; thereafter, it decreased gradually to the same level as in January/February. RR was highest from May to August and lowest in January/February. Fig. 3 shows the combined effect of housing system (for boars) and mating month (2month periods) on total number of piglets born per litter (NTB-m) and on remating (RR). In the CONV system, NTB-m was lowest in September/October (rainy season), while in the EVAP system NTB-m was highest from September to December. RR was highest in November/December (winter season) and lowest in March/April (hot season) in the CONV system; RR was highest in July/August (rainy season) and lowest from November to February (winter season) in the EVAP system. The maximum numeric differences between the housing systems (for boars) were not significant, being 0.9 piglets (EVAP system was

618

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

Fig. 3. Combined effect of system and mating month on total number of piglets born per litter and on remating rate. LSmeans with one letter in common are not significantly different (P > 0.05). ( ) CONV; ) EVAP; ( ) hot season; ( ) rainy season; ( ) winter season. (

higher) for NTB-m in September/October, and 4.2% (EVAP system was lower) for RR in November/December. 3.3. Effect of temperature and humidity The averages of moving averages of daily maximum temperatures per T-class were as follows: T1, 31.2 8C; T2, 34.2 8C; T3, 36.5 8C. The corresponding averages of moving averages of daily minimum humidity per H-class were: H1, 40% RH; H2, 48% RH; H3, 59% RH. In some herds, there were no observations in some classes of moving average of temperature and humidity. Fig. 4 shows the effect of temperature and humidity on the reproductive variables analyzed (14 days before farrowing: NTB-f, NBA, NSB, and AVBWT; 14 days before weaning: WSI, WSI7, and NTB-w; 14 days after the first service after weaning: NTB-m). T had a significant effect on all reproductive variables (P < 0.05), except on RR (Table 3b). Humidity itself had a significant effect on NTB-f (P < 0.001), NTB-w (P < 0.05), NTB-m (P < 0.05), and NBA (P < 0.01). NTB-w decreased when temperature increased (P < 0.001) from T1 to T2 (on average, 31.2–34.2 8C) and when humidity increased (P < 0.05) from H1 to H3 (on average, 40–59% RH). NTB-m decreased (P < 0.01) when temperature increased from T1 to T2 (on average, 31.2– 34.2 8C), and increased again from T2 to T3 (on average, 34.2–36.5 8C). NTB-m decreased (P < 0.05) when humidity increased from H1 to H3 (on average, 40–59% RH). NBA decreased (P < 0.05) when temperature increased from T2 to T3 (on average, 34.2– 36.5 8C), and decreased (P < 0.01) when humidity increased from H1 to H2 (on average,

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

619

Fig. 4. Influence of temperature and humidity on the reproductive performance in sows. LSmeans with one letter ) Temperature (T); ( ) humidity (H). in common are not significantly different (P > 0.05). (

40–48% RH). NSB (P < 0.001) and AVBWT (P < 0.001) increased when temperature increased from T2 to T3 (on average, 34.2–36.5 8C), and from T1 to T2 (on average, 31.2– 34.2 8C), respectively. WSI increased (P < 0.001) when temperature increased from T1 to T2 (on average, 31.2–34.2 8C), and decreased again from T2 to T3 (on average, 34.2– 36.5 8C). WSI7 displayed a pattern opposite to that of WSI. The interaction between parity and temperature also had a significant effect on all reproductive variables analyzed

620

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

(P < 0.05), except on NTB-m, WSI7, and RR (Table 3b). The interaction between parity and humidity had a significant effect on NTB-f (P < 0.001), NBA (P < 0.001), AVBWT (P < 0.001), and RR (P < 0.05). In general, primiparous sows were more sensitive to high temperature and high humidity at farrowing than elder sows were. The LSmeans of NBA and NSB at T1 and T3 in primiparous sows were 9.3 and 9.1 piglets, and 0.6 and 0.8 piglets, respectively; in sow parity numbers 6–8, these values were 10 and 10.1 piglets, and 0.9 and 0.9 piglets, respectively. Corresponding LSmeans of NBA at H1 and H3 in primiparous sows were 9.5 and 9.2 piglets, respectively; in sow parity numbers 6–8, these values were 10.1 and 10 piglets, respectively. However, the combined effects of parity and temperature, and of parity and humidity, largely only describe the independent effect of parity. Fig. 5 shows the combined effect of temperature and humidity on the reproductive performance variables analyzed, after omission of the combinations including T2 or H2. The interactions between temperature and humidity were in most cases not significant or only weakly significant, and the combined effects in most cases only describe the independent effects of T and H. However, the interaction between T and H was significant (P < 0.001) for NTB-f, NBA, and AVBWT (Table 3b). The combination of T3 and H3 seems to be negative for NTB-f, NTB-w, and NBA, but seems to be positive for AVBWT. Sometimes inconsistent non-significant decreases and/or increases in WSI, WSI7, and RR were found when the effect of temperature was combined with the effect of humidity: low– low (T1H1), low–high (T1H3), high–low (T3H1), and high–high (T3H3), respectively (data

Fig. 5. Combined effect of classified temperature and humidity on reproductive performance in sows. Significant differences between LSmeans are shown in the diagram. The combinations including T2 or H2 are omitted from this presentation.

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

621

not shown). The proportion of observations in each of these combinations was approximately 10% of the total number of observations. The interactions between housing system (for boars) and temperature for RR (P < 0.001), and between system and humidity had significant effects on NTB-w (P < 0.05) and NTB-m (P < 0.01) (Table 3b). Fig. 6 shows the combined effects of housing system (for boars) and temperature, and of housing system (for boars) and humidity. In the EVAP system, there was a numerically higher NTB-m for all temperature and humidity classes than in the CONV system. RR was lower in the EVAP system than in the CONV system in temperature class T1, but higher in temperature class T3. The maximum numeric differences (however, not significant) between housing systems (for boars) for NTB-m and RR for temperature (T1) were 0.5 piglet and 3.9%, respectively, and for humidity were 0.5 piglet (H3) and 1.9% (H2), respectively. 3.4. Regular/irregular rematings Forty-six percent of the remated sows were remated with regular return (18–24 or 39–45 days), and 54% with irregular return (25–38 or 46–100 days) remating. Chi-square analysis showed no significant difference in the proportion of regular/irregular return between parities over the three seasons (P = 0.07). However, in the hot season there was a higher (P < 0.01) proportion of irregular return in parities 1, 4–5, and 6–8 (56.1, 54.9, and 57.4%, respectively) compared with parities 2 and 3 (49.3 and 46.4%).

Fig. 6. Combined effect of system and temperature and system and humidity on number of total born piglets per litter and on remating rate. LSmeans with one letter in common are not significantly different (P > 0.05). ( ) CONV; ( ) EVAP.

622

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

4. Discussion The present study investigated the effects of season, temperature, humidity, parity number, lactation length, and housing system (for boars: CONV and EVAP system) on reproductive performance in crossbred sows under tropical climatic conditions. The overall results of the present study reveal that not only elevated temperature but also elevated humidity has a negative impact on reproductive performance in sows. The study was carried out under tropical climatic conditions, meaning high temperature and humidity, which differ markedly from the temperate climatic conditions of northern Europe and the USA. Thus, the temperatures examined in this study were relatively high in all seasons – unlike the prevailing temperatures in previous field studies in both northern Europe [5,6,11] and the USA [3,23–25] – and in the present study the lowest moving average of daily maximum temperature was 26 8C. Moreover, in the present study temperature and humidity were recorded daily inside the herd buildings, whereas in previous field studies only general climatic records were collected from meteorological stations [10,13]. Furthermore, the litter size examined in the present study was relatively low (approximately 1 piglet per litter) compared to the litter sizes examined in studies mainly of crossbred pigs in northern Europe [6] and in the USA [3,23–25]. Similar differences in litter size were reported between studies of purebred pigs (e.g. Landrace and Yorkshire) in Thailand [10,13] and in northern Europe [11]. This might be explained by the difference in climatic conditions, in particular, high temperature and high humidity. The litter size of crossbred sows examined in the present study was higher (approximately 1 piglet per litter) than in previous studies of purebred sows in Thailand [10,13]. This difference might be explained by heterosis effects. 4.1. Parity influence The results of the present study show that parity number had a strong influence on litter size, WSI, WSI7, and RR (Fig. 1). A significant increase in litter size was observed from parities 1 through 4–5, followed by a decrease in parities 6–8, which is in accordance with earlier studies [10,11,13]. The increase in litter size from parities 1 through 4–5 might be explained by an increase in ovulation rate, uterine capacity [26], and age of sow [27]. The longer WSI in primiparous than in multiparous sows found in the present study is in agreement with other studies [1,3,10,11,13]. Inadequate voluntary feed intake during lactation is found to prolong WSI [28,29], and this occurs especially in primiparous sows [29]. As a consequence of this, primiparous sows use more of their own body reserves for milk production than multiparous sows do [30,31]. WSI7 was lowest in primiparous sows in the present study. This is in agreement with the result of another study [31], which reported that a large body weight loss during lactation in primiparous sows reduces their ability to return to estrus within 10 days after weaning. The present study found primiparous sows to have a significantly higher RR than multiparous sows did, which also is in agreement with some earlier studies [1,11,23,32]. One factor contributing to this difference might be a higher risk of suboptimal insemination time due to shorter estrus in primiparous than in multiparous sows [33].

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

623

4.2. Effect of season The present study showed that season (2-month periods) significantly influenced all traits analyzed. The pattern of seasonal effect on reproductive performance in Thailand (tropical area) differs from that found in northern Europe and USA. This might be explained by the differences in seasons (in terms of temperature and photoperiod), with three seasons in Thailand (hot season: March to June; rainy season: July to October; winter season: November to February), and four seasons in northern Europe and the USA (winter season: December to February; spring: March to May; summer: June to August; autumn: September to November). Artificial cooling (e.g. water sprinkling, fogging, and fans) was sometimes used for the sows (not recorded) when the temperature was considered to be too high. Thus, the temperature and humidity recorded in the present study might deviate somewhat from corresponding parameters recorded at meteorological stations. In Thailand, day length is almost equal throughout the year, being approximately 12  1 h. Therefore, the seasonal variation in reproductive performance in sows in this study can be regarded as caused mainly by variations in temperature and humidity. NTB-f and NTB-m were highest when the sows were mated during the winter season (Fig. 2), when the temperature is lower than in other seasons. High ambient temperature has been reported to deleteriously affect reproduction in sows, either by acting directly on ovarian function or via the hypothalamic-pituitary-ovarian axis [12,34–36]; high temperature could also affect spermatogenesis in boars [37,38]. The smaller litter size found by this study might be explained by a poor fertilization rate, high embryonic death, and/or lower semen quality. Moreover, NTB-f was lower than NTB-m in all seasons, which is explained by the inclusion of first parity litters in NTB-f. RR was found to be higher for sows mated during May to August. This might be explained by lower frequency of morphologically normal spermatozoa in ejaculates from July/ August than from either the hot season or winter season [39]. The results obtained agree in principle with those of some previous studies, showing decreased litter size [24,40] and increased RR in the northern hemisphere [24,41]. However, there is controversy concerning the influence of season on litter size. Some studies find no variation in litter size due to season. However, most of those studies were done in temperate or subtropical areas where the ambient temperature may not play a major role in seasonal variation in reproductive performance [4,6,11,42]. In the present study, there was also a significant interaction between housing system (for boars) and 2-month periods on NTB-m and RR, which indicates differences between seasonal variations in the quality of semen from the boars in the two housing systems. NTB-m was highest when mating occurred in September/October (rainy season) in the EVAP system, but lowest if mated in the same period in the CONV system (Fig. 3). RR was higher in the CONV system than in the EVAP system from September/October (rainy season) until January/February (winter season). The reason for the lower litter size and higher RR in the rainy season in the CONV system than in the EVAP system might be the difference in semen quality. This is in agreement with a previous study [39] of these 11 herds, which reported that during the rainy season a higher proportion of ejaculates from boars kept in the CONV system had less than 60% morphologically normal

624

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

spermatozoa than did ejaculates from boars kept in the EVAP system (19.1% versus 10.4%). An increase in WSI was found when sows were weaned in the hot season (May/June), and this increase continued into the rainy season (September/October). This is in agreement with the findings of some earlier studies conducted in temperate and tropical areas, showing a prolonged WSI when weather is hot [2,4,10,42]. A prolonged WSI when weather is hot has been reported to be partly associated with reduced appetite, and/or energy and protein deficit [43,44], or with limitations of feed allowance during lactation [45]. The present study showed that lactation length had a strong influence on subsequent litter size (NTB-w and NTB-m), WSI, and WSI7. A significant increase in litter size and decrease in WSI was observed when LL increased (from 16–21 to 27–35 days), which is in accordance with earlier studies [3,25,46–49]. Sows with longer lactation periods may have more time to balance their metabolic status, leading to a shorter interval from weaning to estrus [50]. There were higher incidences of irregular rematings in the hot season than in other seasons in sows of parity numbers 1, 4–5, and 6–8. This could be because higher temperature and lower humidity in the hot season disturbed the ovarian function (e.g. caused cystic ovaries) and/or increased embryonic death around implantation time in these categories of sows. Regular return after the first service might, on the other hand, indicate management problems such as suboptimal estrus checking and/or insemination technique. Thus, one must consider that remating problems might be caused by other factors than simply problems related to the sows or poor semen quality. 4.3. Effect of temperature and humidity Maximum temperature and minimum humidity were chosen as microclimatic indicators when analyzing the climatic effect on reproductive performance in sows, because the maximum temperature usually occurs contemporary with minimum humidity in early afternoon. From a human perspective, this is felt to be the hottest time of day [51]. To our knowledge, no study of the direct effect of temperature and humidity (based on daily measurements made within the herd) on reproductive performance of sows has been performed under tropical conditions. This study shows a significant influence of both the 14-day moving average of maximum temperature and the 14-day moving average of minimum humidity on several reproductive parameters in the sows (Table 3b). In most cases, increased temperature and humidity had a negative effect on litter size (Fig. 4). The decrease in litter size caused by increased maximum temperature, we found, was not consistent with the reported findings of another field study in Thailand [10], which reported a 0.07-piglet decrease per litter for each 1 8C temperature increase. This difference in results might be explained by the different temperature recording methods used: temperature was recorded within the herd in the present study, but at meteorological stations in the previous field study. Increased humidity, recorded within the herd in the present study, showed a more consistent negative effect on litter size (Fig. 4). Humidity higher than H1 (average, 40% RH) both during lactation (before weaning) and after mating, respectively, caused

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

625

decreased NTB-w and NTB-m. The mechanism behind the negative effect of humidity is not fully understood, but might be connected with discomfort and/or heat stress for the sows. It has been reported that at temperatures above 31 8C, a 10% increase in relative humidity is equivalent to a 1 8C rise in air temperature [51], and heat stress can negatively affect follicular growth (resulting in decreased number of ovulations) and/or increase early embryonic death [15,19]. Both increased temperature and increased humidity in the late gestation period decreased NBA in the present study. This is in accordance with the results of an experimental study showing that pregnant sows exposed to heat stress in the late gestation period farrowed fewer live-born and more stillborn piglets than did sows kept at a comfortable temperature [15]. The combined effects of temperature and humidity were also studied (Fig. 5). As is evident from this figure, there were no significant differences in litter size between the combinations low temperature and high humidity (T1H3), and high temperature and low humidity (T3H1). However, the combination of high temperature (T3) and high humidity (H3) had a significant negative effect on litter size. These results indicate that sows have a certain capacity to adapt to elevated temperature or elevated humidity, but less capacity to adapt to the combination of elevated temperature and elevated humidity. For other recorded reproductive parameters (e.g. WSI, WSI7, and RR), no consistent influence pattern of combination of temperature and humidity could be detected. In the present study, temperature was quite high in the stables in all the seasons (the range of the moving average of daily maximum temperature was 26–41 8C), much higher than the temperatures examined in corresponding field studies conducted in the northern hemisphere [6,11,12]. When temperature was considered to be too high for the sows, artificial cooling was sometimes applied by means such as water sprinkling, fogging, and fans. These methods might have somewhat inflated the magnitude of maximum temperature and minimum humidity in the herds, and might have reduced the harsh effect of high temperature on reproductive parameters. Moreover, NTB-m was numerically higher in all temperature and humidity classes in the EVAP system than in the CONV system (Fig. 6). The reason for this is not clear, because the housing system (for boars) had no overall effect on any reproduction parameter investigated (Table 3b). One factor contributing to this lack of overall effect might be the limited number of herds, within each system, examined in the present study. To minimize the negative impact of high temperature and high humidity on sperm production in boars and reproductive performance in sows under tropical climate, further investigations on economically competitive technologies that can decrease temperature and humidity is needed.

5. Conclusions - No significant differences were found in the reproductive performance of sows inseminated with semen from boars kept in two different housing systems (CONV or EVAP system). - Seasonal variation in reproductive performance of sows was found.

626

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

- There were indications that high temperature and humidity (recorded within the herd) at previous weaning/mating or at farrowing had negative effects on litter size. - Further investigation is needed, especially of the effect of humidity on the reproductive performance of sows.

Acknowledgements The Royal Thai Government is acknowledged for their financial support and Chulalongkorn University, Thailand, for granting Annop Suriyasomboon study leave. The authors thank the pig herds involved for providing information for use in this study.

References [1] Claus R, Weiler U. Influence of light and photoperiodicity on pig prolificacy. J Reprod Fertil Suppl 1985;33:185–97. [2] Hurtgen JP, Leman AD, Crabo B. Seasonal influence on estrous activity in sows and gilts. J Am Vet Med Assoc 1980;176:119–23. [3] Koketsu Y, Dial GD. Factors influencing the postweaning reproductive performance of sows on commercial farms. Theriogenology 1997;47:1445–61. [4] Love RJ, Evans G, Klupiec C. Seasonal effects on fertility in gilts and sows. J Reprod Fertil Suppl 1993;48:191–206. [5] Peltoniemi OA, Love RJ, Heinonen M, Tuovinen V, Saloniemi H. Seasonal and management effects on fertility of the sow: a descriptive study. Anim Reprod Sci 1999;55:47–61. [6] Peltoniemi OA, Tast A, Love RJ. Factors effecting reproduction in the pig: seasonal effects and restricted feeding of the pregnant gilt and sow. Anim Reprod Sci 2000;60–61:173–84. [7] Prunier A, Dourmad JY, Etienne M. Effect of light regimen under various ambient temperatures on sow and litter performance. J Anim Sci 1994;72:1461–6. [8] Prunier A, Messias de Braganc¸a M, Le Dividich L. Influence of high ambient temperature on performance of reproductive sows. Livest Prod Sci 1997;52:123–33. [9] Prunier A, Quesnel H, Messias de Braganc¸a M, Kermabon AY. Environmental and seasonal influences on the return-to-oestrus after weaning in primiparous sows: a review. Livest Prod Sci 1996;45:103–10. [10] Tantasuparuk W, Lundeheim N, Dalin AM, Kunavongkrit A, Einarsson S. Reproductive performance of purebred Landrace and Yorkshire sows in Thailand with special reference to seasonal influence and parity number. Theriogenology 2000;54:481–96. [11] Tummaruk P, Lundeheim N, Einarsson S, Dalin AM. Reproductive performance of purebred Swedish Landrace and Swedish Yorkshire sows: I. Seasonal variation and parity influence. Acta Agric Scand Sect A Anim Sci 2000;50:205–16. [12] Wettemann RP, Bazer FW. Influence of environmental temperature on prolificacy of pigs. J Reprod Fertil Suppl 1985;33:199–208. [13] Tummaruk P, Tantasuparuk W, Techakumphu M, Kunavongkrit A. Effect of season and outdoor climate on litter size at birth in purebred Landrace and Yorkshire sows in Thailand. J Vet Med Sci 2004;66:477–82. [14] Gourdine JL, Renaudeau D, Noblet J, Bidanel JP. Effects of season and parity on performance of lactating sows in a tropical climate. Anim Sci 2004;79:273–82. [15] Omtvedt IT, Nelson RE, Edwards RL, Stephens DF, Turman EJ. Influence of heat stress during early, mid and late pregnancy of gilts. J Anim Sci 1971;32:312–7. [16] Quiniou N, Noblet J. Influence of high ambient temperatures on performance of multiparous lactating sows. J Anim Sci 1999;77:2124–34. [17] Renaudeau D, Anaı´s C, Noblet J. Effect of dietary fiber on performance of multiparous lactating sows in a tropical climate. J Anim Sci 2003;81:717–25.

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

627

[18] Renaudeau D, Quiniou N, Noblet J. Effects of exposure to high ambient temperature and dietary protein level on performance of multiparous lactating sows. J Anim Sci 2001;79:1240–9. [19] Tompkins E, Heidenreich CJ, Stob M. Effect of post-breeding thermal stress on embryonic mortality in swine. J Anim Sci 1967;26:377–80. [20] Wettemann RP, Bazer FW, Thatcher WW, Caton D, Roberts RM. Conceptus development, uterine response, blood gases and endocrine function of gilts exposed to increased ambient temperature during early pregnancy. Theriogenology 1988;30:57–74. [21] Simmons JD, Lott BD. Evaporative cooling performance resulting from changes in water temperature. Appl Eng Agric 1996;12:497–500. [22] Suriyasomboon A, Kunavongkrit A, Lundeheim N, Einarsson S. Effect of temperature and humidity on sperm production in Duroc boars under different housing systems in Thailand. Livest Prod Sci 2004;89:19– 31. [23] Koketsu Y, Dial GD, King VL. Returns to service after mating and removal of sows for reproductive reasons from commercial swine farms. Theriogenology 1997;47:1347–63. [24] Xue JL, Dial GD, Marsh WE, Davies PR. Multiple manifestations of season on reproductive performance of commercial swine. JAVMA 1994;204:1486–9. [25] Xue JL, Dial GD, Marsh WE, Davies PR, Lucia T. Association between lactation length and sows reproductive performance and longevity. JAVMA 1997;210:935–8. [26] Gama LL, Johnson RK. Changes in ovulation rate, uterine capacity, uterine dimensions, and parity effects with selection for litter size in swine. J Anim Sci 1993;71:608–17. [27] Culbertson MS, Mabry JW, Bertrand JK, Nelson AH. Breed-specific adjustment factors for reproductive traits in Duroc, Hampshire, Landrace, and Yorkshire swine. J Anim Sci 1997;75:2362–7. [28] Koketsu Y, Dial GD, Pettigrew JE, Marsh WE, King VL. Characterization of feed intake patterns during lactation in commercial swine herds. J Anim Sci 1996;74:1202–10. [29] Whittemore CT. Nutrition reproduction interactions in primiparous sows. Livest Prod Sci 1996;46:65–83. [30] Sterning M, Rydhmer L, Eliasson L, Einarsson S, Andersson K. A study on primiparous sows of the ability to show standing oestrus and to ovulate after weaning. Influences of loss of body weight and backfat during lactation and of litter size, litter weight gain and season. Acta Vet Scand 1990;31:227–36. [31] Neil M, Ogle B, Anner K. A two-diet system and ad libitum lactation feeding of the sow. 1. Sow performance. Anim Sci 1996;62:337–47. [32] Clark LK, Schinckel AP, Singleton WL, Einstein ME, Teclaw RF. Use of farrowing rate as a measure of fertility of boars. JAVMA 1989;194:239–43. [33] Steverink DW, Soede NM, Groenland GJ, van Schie FW, Noordhuizen JP, Kemp B. Duration of estrus in relation to reproduction results in pigs on commercial farms. J Anim Sci 1999;77:801–9. [34] Armstrong JD, Britt JH, Cox NM. Seasonal differences in function of the hypothalamic-hypophysial-ovarian axis in weaned primiparous sows. J Reprod Fertil 1986;78:11–20. [35] Foxcroft GR. Nutritional and lactational regulation of fertility in sows. J Reprod Fertil Suppl 1992;45:113–25. [36] Quesnel H, Pasquier A, Mounier AM, Prunier A. Influence of feed restriction during lactation on gonadotropic hormones and ovarian development in primiparous sows. J Anim Sci 1998;76:856–63. [37] Cameron RD, Blackshaw AW. The effect of elevated ambient temperature on spermatogenesis in the boar. J Reprod Fertil 1980;59:173–9. [38] Malmgren L. Experimentally induced testicular alterations in boars: sperm morphology changes in mature and peripubertal boars. J Vet Med Ser A 1989;36:411–20. [39] Suriyasomboon A, Kunavongkrit A, Lundeheim N, Einarsson S. Effect of temperature and humidity on sperm morphology in Duroc boars under different housing systems in Thailand. J Vet Med Sci 2005;67, in press. [40] Yen HF, Isler GA, Harvey WR, Irvin KM. Factors affecting reproductive performance in swine. J Anim Sci 1987;64:1340–8. [41] Elbers ARW, van Rossern H, Schukken YH, Martin SW, van Exsel ACA, Friendship RM, et al. Return to oestrus after first insemination in sow herds (incident, seasonality, and association with reproductivity and some blood parameters). Vet Q 1994;16:100–9. [42] Love RJ, Klupiec C, Thornton EJ, Evans G. An interaction between feeding rate and season affects fertility of sows. Anim Reprod Sci 1995;39:275–84.

628

A. Suriyasomboon et al. / Theriogenology 65 (2006) 606–628

[43] King RH. Nutritional anoestrus in young sows. Pig News Info 1987;8:15–22. [44] Dourmad JY, Etienne M, Prunier A, Noblet J. The effect of energy and protein intake of sows on their longevity: a review. Livest Prod Sci 1994;40:87–97. [45] Messias de Braganc¸a M, Mounier AM, Prunier A. Does feed restriction mimic the effects of increased ambient temperature in lactating sows? J Anim Sci 1998;76:2017–24. [46] Clark LK, Leman AD. Factors that influence litter size in pigs. Pig News Info 1986;7:303–10. [47] Koketsu Y, Dial GD. Interactions between the associations of parity, lactation length, and weaning-toconception interval with subsequent litter size in swine herds using early weaning. Prev Vet Med 1998;37:113–20. [48] Mabry JW, Culbertson MS, Reeves D. Effects of lactation length on weaning-to-first-service interval, firstservice farrowing rate, and subsequent litter size. J Swine Health Prod 1996;4:185–8. [49] Tummaruk P, Lundeheim N, Einarsson S, Dalin AM. Reproductive performance of purebred Swedish Landrace and Swedish Yorkshire sows: II. Effect of mating type, weaning-to-first-service interval and lactation length. Acta Agric Scand Sect A Anim Sci 2000;50:217–24. [50] Hulte´n F, Neil M, Einarsson S, Ha˚kansson J. Energy metabolism during late gestation and lactation in multiparous sows in relation to backfat thickness and the interval from weaning to first oestrus. Acta Vet Scand 1993;34:9–20. [51] Steadman RG. The assessment of sultriness. Part I. A temperature–humidity index based on human physiology and clothing science. J Appl Meteor 1979;18:861–73.