The effect of birth weight and age at tail docking and ear notching on the behavioral and physiological responses of piglets1 K. E. Bovey,* T. M. Widowski,* C. E. Dewey,* N. Devillers,† C. Farmer,† M. Lessard,† and S. Torrey*†2,3 *University of Guelph, Guelph, Ontario, Canada, N1G 2W1; and †Agriculture and Agri-Food Canada, Sherbrooke, Québec, Canada, J1M OC8

ABSTRACT: Selection for high prolificacy has resulted in litters comprising a large number of low-birth-weight (LBW) piglets. Given their presence in over 75% of litters and increased mortality rate, it is clear that a greater understanding of LBW piglet management is required for both animal welfare and productivity. In this study, we compared the effects of tail docking and ear notching LBW and average-birth-weight (ABW) piglets at 1 or 3 d of age on suckling, behavior, passive transfer of immunoglobulins, and growth. Six piglets per litter from 20 litters (n = 120 piglets) were used in a 2 × 2 complete block design. Piglets were weighed at birth and designated as LBW (0.6 to 1.0 kg) or ABW (≥1.2 kg) and “processed” (tail docked and ear notched) at either 1 or 3 d of age. Vocalizations were recorded during the procedures. The acute behavioral responses were observed for 10 min after the procedure. Piglets were observed for 6 h after birth and after the procedure to determine their presence at nursing bouts. On d 5, blood samples were collected to determine concentrations of serum immunoglobulins (IgA and IgG) and IGF-I. Piglet weights were recorded at birth and on d 5, 14, and 21. During the pro-

cedures, LBW piglets produced fewer (P = 0.03) calls than ABW piglets. Piglets from either birth weight category produced a similar number (calls/s; P = 0.29) of high-frequency calls (≥1,000 Hz), which are indicative of pain and distress, although the average frequency (Hz) of these calls was greatest (P = 0.05) for ABW piglets processed on d 3. Immediately following the procedures, LBW piglets spent more (P = 0.005) time dog-sitting and less (P = 0.005) time lying than ABW piglets. When observed with the sow, LBW males spent more (P = 0.001) time alone and had the lowest (P = 0.007) attendance at nursing bouts compared with LBW females and all ABW piglets. Concentrations of serum IgA (P = 0.06) and IgG (P = 0.04) and plasma IGF-I (P = 0.003) were lower for LBW than ABW piglets regardless of age of processing although the magnitude of these differences was likely not of biological significance. Average-birthweight piglets may be less reactive to the acute effects of the procedures on d 1 than on d 3. Given the decreased likelihood of a LBW piglet surviving to weaning (P = 0.001), delaying processing until 3 d of age for LBW piglets may eliminate unnecessary procedures.

Key words: behavior, birth weight, neonate, pain, piglet, vocalizations © 2014 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2014.92:1718–1727 doi:10.2527/jas2013-7063 INTRODUCTION

1This research project was funded by AAFC-AAC. The authors wish to acknowledge the technical assistance of K. Morrissey, K. Radziszewska, A. Arnone, A. Dicks, L. Thibault, L. Marier, and P. Alphée Plante during data collection and analyses and S. Méthot for assistance with statistical analyses. Special thanks to Brian Dunk for use of his facilities and manpower. 2Present address: Agriculture and Agri-Food Canada, Department of Animal and Poultry Science, University of Guelph, Guelph, ON, N1G 2W1, Canada. 3Corresponding author: [email protected] Received August 22, 2013. Accepted January 4, 2014.

Modern genetic lines of swine have favored maternal fecundity. Between 2005 and 2011, average litter size has increased by 0.2 piglets per year in the United States, with 10% of litters having over 12.5 live born piglets (Pig Champ, 2011). However, total litter weights have not increased proportionally. When litter size increased from less than 11 to over 15 piglets, average birth weight (ABW) was reduced by more than 300 g and the percentage of low-birth-weight (LBW) piglets (≤1.0 kg) increased from 7 to 23% (Quiniou et al., 2002). Through the first week of postnatal life,

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LBW piglets have low survival rates (Marchant et al., 2000) although labor-intensive intervention techniques including the drying and warming of recently farrowed piglets and supplemental food provision has been shown to increase their survival rates (Dewey et al., 2008). On the majority of North American farms, surgical procedures, including tail docking and castration, are routinely performed within the first 3 d after birth. This coincides with a critical period for piglet survival, when immunoglobulin-rich colostrum is available and normal suckling behavior is established (Fraser, 1980; Le Dividich et al., 2005). The impact of these procedures on ABW piglets may include pain for up to 3 d after the procedure (Hay et al., 2003), isolated behavior (Llamas Moya et al., 2008), and suckling for decreased periods with a greater incidence of missed nursing bouts (McGlone et al., 1993) although not always (Torrey et al., 2009). The effects of such routine procedures on suckling and milk intake have not been studied for the more vulnerable LBW piglets. Therefore, the objective of this experiment was to compare the effects of tail docking and ear notching LBW and ABW piglets during the first 24 h postpartum versus at 3 d of age on suckling, passive transfer of immunoglobulins, behavior, and growth. MATERIALS AND METHODS This experiment took place between May and August 2009 at a commercial farrowing facility located near Guelph, Ontario, Canada. All procedures in this study were approved by the University of Guelph Animal Care Committee in accordance with guidelines outlined by the Canadian Council on Animal Care. Experimental Design One hundred twenty (Yorkshire × Landrace) × Duroc piglets from 20 naturally farrowed litters (6 piglets per litter) were used in this experiment. Litters were born to sows with an average parity of 3.58 ± 1.47 (range: parity 2–7). Litters had 14.00 ± 2.47 live-born piglets (range: 10–18 live-born piglets), with an average birth weight of all piglets in a litter of 1.30 ± 0.34 kg (range: 0.3– 2.0 kg). Piglets were weighed at birth, individually identified, and assessed visually for viability. A piglet was deemed viable when it displayed normal conformation (able to locomote on the pedal surface of the claws; not sternally recumbent or splay legged), normal vigor (responsive to environment/stimuli comparable to conspecifics), and coordination (orientation and/or successful movement toward the most appropriate stimulus). Piglets were assigned to 1 of 2 weight classifications—1) LBW, 0.6 to 1.0 kg (n = 40 piglets), and 2) ABW, ≥1.2 kg (n = 80 piglets)—and 1 of 2 treatment days—1) Downloaded from https://academic.oup.com/jas/article-abstract/92/4/1718/4703441 by University of Adelaide user on 04 May 2018

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d 1 (16.1 ± 1.1 h after birth) and 2) d 3 (63.9 ± 1.1 h after birth). There were a total of 20 LBW and 40 ABW piglets for treatment d 1 and 20 LBW and 40 ABW for treatment d 3. Because each litter served as a complete block, sham processed piglets were not included as controls in this study due to the difficulty of attaining enough litters with at least 4 LBW piglets. Therefore, ABW piglets served as controls. Piglets weighing between 1.0 and 1.2 kg were excluded from the trial to allow for a clear delineation between LBW and ABW piglets. Immediately after birth and before suckling, piglets were dried (Scott Shop Towels; Kimberly-Clark, Boswell, GA), temporarily numbered by birth order (RAIDL Maxi Animal Marking Crayon, Otterbach, Germany), and placed in plastic containers (61 cm length by 40.6 cm width by 31.8 cm height cm; Rubbermaid, Mississauga, ON) containing hot water bottles and absorbent pads (Extra Thick Training Pads; OUT! International Inc., Dallas, TX) that were placed in the farrowing crate. A colostrum sample was collected from at least 2 unsuckled teats of each sow. Once 6 piglets meeting the experimental criteria were born, each was individually identified with numbers hair dyed onto their backs (Herbal Essences Sapphire Black hair dye, Stamford, CT). At this time, all piglets were returned to the sow, in close proximity to the udder, to permit all to begin suckling simultaneously. Time 0 was defined as when all experimental piglets were placed on the udder. Only litters that had 6 viable piglets (including 2 LBW piglets) born within 4 h before time 0 were included in the experiment. Average farrowing duration was 177 ± 55 min. When an experimental piglet died before treatment application, a natural littermate (whose birth weight could be ascertained through the birth order number on its back) was substituted. A subsample of piglets (n = 53; 30 ABW and 23 LBW piglets) from 13 sows were selected at random for anatomical measurements. Crown circumference was determined by placing a soft, flexible measuring tape around the piglet’s cranium so that it was level with the medial canthus, passed medial to the ear pinna, and terminated at the level of the occiput. For determination of crown-to-rump length, a measuring tape was positioned level with the medial canthus and run along the length of the spine to the base of the tail. Body weight and crownto-rump length were used to calculate Ponderal Index (PI), where PI = kilograms per cubic meter. In litters with supernumerary piglets, split-suckling was performed at the first nursing bout for a minimum of 15 min, with experimental piglets being placed at the udder first. The entire litter was left on the sow until the time of first treatment, when some piglets were fostered off to standardize litter size to 11 to 12 piglets. Due to foster sow availability, the litter from 1 experimental sow was kept at 16 pigs until d 4. All piglets received a 1 mL injection of gleptoferron iron (200 mg/mL) intramuscularly in the

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right neck muscle (Gleptosil; Alstoe Ltd. Animal Health, Yorkshire, England, distributed by Champion Alstoe Animal Health Inc., Whitby, ON) on d 5. There were 56 females and 64 males used in the experiment (LBW: 20 females and 20 males; ABW: 36 females and 44 males). Male piglets were castrated on d 14. Mortalities were recorded through to weaning at 22 ± 2 d. Piglet health was monitored on a daily basis. Euthanasia was performed when injury or debilitation prevented locomotion and/or nursing bout attendance and recovery was not likely. Before ear notching and tail docking, the experimental 3 piglets assigned to that processing day were removed from the farrowing crate and moved to the hallway in a plastic container (81.3 cm length by 51.4 cm width by 42.2  cm height; Rubbermaid, Hinged Storage Box, Mississauga, ON) with a heat lamp. One piglet at a time was brought into a separate room, with the door closed to minimize noise disturbance. The order of treatment was alternated between litters of piglets and treatment ages within litters. Tail docking and ear notching of piglets were performed by a trained handler without the use of anesthesia or analgesia as per normal on-farm practice. Piglets were held against the hip of the handler for ear notching. Each piglet received 1 notch in the middle of the base of the right ear using standard stainless steel ear notchers (Kane Veterinary Supplies Ltd., Cambridge, ON). Piglets were then held up by the left hind leg for tail docking. Side-cutter pliers (CDMV, St. Hyacinthe, QC) were used for tail docking, and tails were docked to one-third the original length. Piglets were handled for 31.5 ± 0.66 s. Vocalizations and Behavior During the procedures, piglet vocalizations were recorded using a digital camcorder (Panasonic HCD-HS9 High definition video camera; Matsushita Electric Industrial Co. Ltd., Osaka, Japan) and the audio files were extracted using VLC media player 1.0.2 (VideoLAN, Paris, France). Vocalizations were analyzed using the sound analysis software program Raven Pro 1.2.2 (Cornell Lab of Ornithology, Ithaca, NY). The frequency (Hz) of each vocalization was determined as the frequency with the greatest energy (amplitude). As per Weary et al. (1998), vocalizations were classified as low if their frequency was below 1,000 Hz; otherwise they were classified as high (Fig. 1). The number of vocalizations produced by each piglet during the ear-notching and tail-docking procedures was counted. Vocalizations were considered separate where an audible pause occurred and where the spectrogram displayed the frequency (Hz) as reaching the baseline value. The files from 2 ABW piglets processed on d 1 contained interfering sound and were omitted from analyses.

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Figure 1. Histogram of all piglet vocalizations. Vocalizations were quadramodal with peaks at approximately 500 to 600, 1,800 to 1,900, 2,900 to 3,000, and >8,000 Hz. A trough occurred at approximately 1,000 Hz and vocalizations in this experiment were classified as low if they had a frequency of less than 1,000 Hz and high if their frequency was greater than 1,000 Hz.

Immediately following the ear-notching and taildocking procedure, piglets were video recorded using the abovementioned camcorder while they were still in the plastic container. Observations were made using scan sampling (Lehner, 1996) every 20 s for 10 min and were expressed as a percentage of the behavioral observation category (general or head-specific or tail-specific behavior) over the period (Table 1). Piglet behavior while suckling was video recorded (Panasonic HDC-HS9 High-definition video cameras; Matsushita Electric Industrial Co. Ltd., Osaka, Japan; Digital video recorder PL12016-00-00; i3DVR International Inc., Scarborough, Canada) on a subsample of litters (n = 14) after they were returned to the farrowing crate for an initial 6-h period at 5.0 ± 0.8 h after time 0 and immediately after treatment. Observations were made on all 6 experimental piglets for the first videorecording period and then on the 3 piglets processed on subsequent treatment days. During nursing bouts (defined as when ≥50% of piglets are active at the udder), piglets were observed at 10 s intervals for their presence at the udder and at 1 min intervals for their proximity to conspecifics when no nursing bout was occurring. Growth and Immune Measures Piglets were weighed using a digital scale, precise to 0.1 kg (DYMO 4010; Pelouze Scale Company, Bridgeview, IL), at birth, on d 5 and 14, and at weaning (22 ± 2 d). Blood was collected from each piglet via the periorbital sinus on d 5 using an 18-gauge × 2.2 cm needle (Becton, Dickinson, and Company, Franklin Lakes, NJ). Five milliliters of blood were collected for analyses of IgA and IgG using a vacuum tube without additive (Becton, Dickinson and Company, Franklin Lakes, NJ). An additional 5 mL of blood were collected using an EDTA vacuum tube (Becton, Dickinson and Company) and in-

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Table 1. Ethogram for piglets video recorded immediately following ear notching and tail docking procedures Category Behavior General Standing behavior Lying Huddled

Play/fight

Tail posture

Definition Only the piglet’s feet are in contact with the ground Piglet is laterally or sternally recumbent Bodily contact with at least 1 other piglet and/or standing or hovering over another piglet and/or standing or hovering within half the body length of another piglet’s head A bout of piglet interactions that involves lateral head swiping/biting and/or use of the head to knock/shove and/or rapidly chasing another piglet

Dog-sit

Piglet sitting like a dog, where the hind end/ buttocks are in contact with floor and only the feet of the front legs are in contact with the floor

Escape attempt Other

Piglet attempting to jump up/over wall of observation area Any general behavior not fitting into one of the above categories Tail stump (tail end) maintained in a straightdown direction Tail stump tucked between buttocks Tail stump moving rapidly side to side Piglet moving hind end/buttocks in a side-toside (rubbing) motion while area is pressed to an external surface Head maintained at/near level of spine; piglet not performing any of the behaviors listed below Head moving rapidly in a tilt or side-to-side motion Piglet attempting to scratch ears with hind foot Involuntary muscle tremors; shivering

Normal Jam/hide Wag Scratch

Head/body Normal posture Shake Scratch Tremble

verted immediately to prevent coagulation, to determine concentrations of IGF-I. Each IGF-I sample was centrifuged within 20 min of collection at 3,000 × g for 12 min 4 °C and then the plasma was pipetted into a 5-mL polypropylene tube (Fisherbrand, Fisher Scientific, Markham, ON) and stored at –20°C until analyzed. The IgG and IgG blood samples were refrigerated at 4°C for 24 h and then centrifuged at 3,000 × g for 12 min at 4°C to collect the serum. Each serum sample was pipetted into two 1.5-mL snap-cap microcentrifuge tubes (Fisherbrand, Fisher Scientific, Markham, ON), and frozen at –20°C. Colostrum samples were collected into 128-mL disposable specimen containers (Fisherbrand; Fisher Scientific, Markham, ON). Each sample was grossly filtered through unfolded gauze and stirred on a magnetic plate for 10 min, placed in two 20-mL polypropylene centrifuge tubes (Fisherbrand; Fisher Scientific), and frozen at –20°C. Lactoserum was obtained from colostrum after two 60-min centrifugations at 50,000 × g at 4°C. Concentrations of IGF-I were measured with a commercial kit for humans (Alpco 26-G, Salem, NH) with small modifications as detailed previously (Plante et al., 2011). Validation for a serum pool from lactating sows was demonstrated. Parallelism was 101.2% and average mass recovery was 101.3%. Sensitivity of the assay was 0.10 ng/mL. The intra- and interasDownloaded from https://academic.oup.com/jas/article-abstract/92/4/1718/4703441 by University of Adelaide user on 04 May 2018

say CV were 2.1 and 8.8%, respectively. Blood serum and colostrum samples were analyzed for IgA using an ELISA Quantification Kit (Bethyl Laboratories Inc., Montgomery, TX). Intra-assay CV was 4.64% for colostrum and 3.87% for serum. Blood serum and colostrum samples were analyzed for IgG using an ELISA Quantification Kit (Bethyl Laboratories Inc., Montgomery, TX). Intra-assay CV was 3.47% for colostrum and 4.36% for serum. Statistical Analyses Data were analyzed using SAS-PC System Version 9.1 for Windows (SAS Inst. Inc., Cary, NC). The main effects tested were birth weight classification, day of treatment, sex, and the interactions. Litter was used as a random effect. General linear models with arcsine transformations were used for analyses of piglet body measurements and immediate behavioral effects of ear notching and tail docking. The mixed model procedure was used for analyses of vocalizations, suckling behavior, growth, IGF-I, and immune measures. Mortality data were analyzed using chi-square and odds ratio. For suckling behavior and growth rates, data were analyzed as repeated measures. For suckling behavior, processing day was omitted from the analysis and those processed on different days were analyzed separately. This was necessary because, other than immediately postnatal, suckling behavior was only observed on the day piglets were processed. When interactions were significant (P < 0.10), the main effects of treatment were separated using contrasts. Main effects and interactions between main effects were included in the initial statistical model and removed when P > 0.10. True means and standard errors are reported. For analyses of IgA and IgG, correlations were performed between blood and colostrum samples to determine if colostrum concentrations needed to be included as covariates. Concentrations of IgA in serum and colostrum were highly correlated (P < 0.0001); therefore, colostrum concentrations were used as a covariate in serum analyses. Concentrations of IgG in serum and colostrum tended to be correlated (P = 0.09) and colostrum concentrations were also used as covariates in serum analyses. RESULTS Anatomical Measurements Larger (P < 0.0001) crown circumference values (ABW: 18.4 ± 0.2 cm; LBW: 17.0 ± 0.1 cm) and crownto-rump length (ABW: 33.7 ± 0.4 cm; LBW: 29.5 ± 0.4 cm) were found in ABW than in LBW piglets. Lowbirth-weight piglets had a larger (P = 0.013) mean value for the ratio of crown to crown-to-rump measures (ABW: 0.55 ± 0.1; LBW: 0.58 ± 0.1) and a smaller (P = 0.01)

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Figure 3. Mean frequency (mean Hz ± SE) of vocalizations greater than 1,000 Hz during ear notching and tail docking by birth weight and processing day. Average frequency was lowest for average-birth-weight (ABW) piglets processed at 1 d of age and highest for ABW piglets ear notched and tail docked at 3 d (P < 0.05). LBW = low birth weight.

Figure 2. Mean call rate (mean calls/s ± SE) for low-birth-weight (LBW) or average-birth-weight (ABW) piglets ear notched and tail docked at 1 or 3 d of age. Rates are shown separately for (a) all calls and (b) low calls ( 0.32) on time spent in proximity to the sow between nursing bouts for piglets processed at either age. However, piglets spent more time in proximity to the sow immediately postnatal than after processing on d 1 (P = 0.01) or d 3 (P < 0.0001). Growth Rates and Mortalities During the course of the experiment, 9 experimental piglets died and 10 were euthanized. Of the 19 mortalities, 9 occurred before treatment: 5 occurred at less than 24 h of age and were replaced in the trial with littermates; 4 occurred at less than 72 h of age and were not substituted with littermates. Of the total mortalities, 6 were ABW and 13 were LBW (P = 0.0007). Only 2 of the 19 total mortaliDownloaded from https://academic.oup.com/jas/article-abstract/92/4/1718/4703441 by University of Adelaide user on 04 May 2018

Table 2. Effect of birth weight (low or average birth weight) on ADG (mean ± SE) through 21 d of age Weight treatment Low birth weight Average birth weight a,bWithin

n 40 80

Birth to 5 d 81.6 ± 8.9a 150 ± 5.8b

ADG, g/pig∙d 5 to 14 d 14 to 21 d 161.8 ± 11.8a 218.9 ± 7.8a 246.1 ± 5.6 b 269 ± 7.1b

columns, a ≠ b, P < 0.01.

ties were female (P = 0.001), both of which were LBW. When cause of death was not readily apparent, the carcass was submitted for histopathological analyses (Animal Health Laboratory, University of Guelph, Guelph, Ontario). All 6 of the ABW mortalities resulted from crushing by the sow. Causes of death/humane endpoint determinations for LBW piglets occurred for various reasons: starvation in combination with chilling or injury (8 piglets), crushed by sow (2 piglets), severe injury (1 piglet), polyarthritis (1 piglet), and septicemia (1 piglet). More (P = 0.007) LBW piglets (7) than ABW piglets (3) died after processing and more (P = 0.05) piglets processed on d 1 died (8) compared with piglets processed on d 3 (2). Body weights and ADG differed between birth weight category (P < 0.0001), age at weighing (P < 0.0001), and the birth weight category and age at weighing interaction (P < 0.0001; Table 2). No differences in BW were found for age at processing (P = 0.46) or age at processing by birth weight (P = 0.83). Insulin-Like Growth Factor-I Concentrations and Immune Measures The average concentration of IGF-I in piglet plasma on d 5 was 52.3 ± 2.0 ng/mL (range: 7.4 to 126.2 ng/mL). There was an effect (P = 0.0005) of birth weight class on IGF-I concentrations but no effect (P = 0.13) of age at processing (Fig. 4a). The concentration of IgA in colostrum was 12.6 ± 0.9 mg/mL (range: 7.7 to 19.1 mg/mL), and the concentration in piglet serum on d 5 was 2.3 ± 0.1 mg/mL (range: 0.9 to 5.0 mg/mL). There was a tendency for an effect (P = 0.06) of piglet weight class on serum concentrations of IgA but no effect (P = 0.48) of age at processing (Fig. 4b). The mean concentration of IgG in colostrum was 71.3 ± 11.6 mg/mL (range: 20.0 to 176.0 mg/mL). Average piglet serum concentration of IgG on d 5 was 30.5 ± 1.0 mg/mL (range: 8.6 to 68.0 mg/mL). There was an effect (P = 0.05; Fig. 4c) of weight class and a tendency (P = 0.08) for a weight class × sex interaction, with LBW females having the lowest serum IgG levels (ABW females: 32.6 ± 1.5 mg/mL; ABW males 30.7 ± 1.5 mg/mL; LBW females 25.8 ± 3.0 mg/mL; LBW males 30.6 ± 2.8 mg/mL). There was no effect (P = 0.59) of age at processing on serum IgG.

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portion of each litter (Milligan et al., 2002). Given the greater LBW piglet mortality in the first week after birth (Marchant et al., 2000), it is clear that the topic of LBW piglet management warrants investigation. In the present study, we evaluated the behavioral and physiological effects of processing LBW piglets at 2 ages. Anatomical Measurements The fact that crown circumference and crown-torump length measures were greater for piglets of heavier birth weight indicated that LBW piglets in this study were of smaller stature than their ABW counterparts. Although these LBW piglets appeared morphologically normal, the greater mean crown:crown-to-rump length ratio and lower mean PI provide evidence to suggest otherwise. Simply stated, LBW piglets had larger heads with proportionately shorter and smaller bodies than their ABW counterparts. These data classify the LBW piglets as displaying asymmetric intrauterine growth retardation (aIUGR; Kramer et al., 1989). The implication of these findings is that the subsample of LBW piglets differed from ABW conspecifics not only in body mass but also in physiology. As summarized by Wu et al. (2006), aIUGR is primarily a result of insufficient nutrient supply from the placenta and is characterized by disproportionate growth of the brain at the expense of vital organ development. Those affected may have altered skeletal muscle composition and exhibit reduced growth performance, organ dysfunction, and increased mortality and morbidity (Wu et al., 2006). The aforementioned differences, in addition to the increased solitary behavior and lack of attendance at nursing bouts, may have contributed to their increased mortality rate in the present study. Vocalizations

Figure 4. Effect of birth weight and day of processing on IGF-I, IgA, and IgG. Mean concentrations (±SE) are shown separately for (a) plasma IGF-I (ng/ mL), (b) serum IgA (mg/mL), and (c) serum IgG (mg/mL) for piglets at 5 d of age, which had been processed at either 1 or 3 d of age and had either low birth weight (LBW) or average birth weight (ABW). Low-birth-weight piglets had lower concentrations of IGF-I (P < 0.001) and IgG (P < 0.05) and a tendency for lower concentrations of IgA (P < 0.10) than ABW piglets. Within main treatment, columns differ: **P < 0.01, *P < 0.05, and †P < 0.10.

DISCUSSION Previously, no research had been done focusing specifically on the effects of processing on LBW piglets. However, with genetic emphasis on sow fecundity, total litter weight is not increasing proportionally, and LBW piglets are representing a greater and greater proDownloaded from https://academic.oup.com/jas/article-abstract/92/4/1718/4703441 by University of Adelaide user on 04 May 2018

Previous studies examining responses to routine surgical procedures have shown vocalizations with frequencies of >1,000 Hz to be reliable indicators of pain and distress in piglets (Weary et al., 1998). In accordance, over 85% of piglets in the current study produced vocalizations >1,000 Hz during the procedures, providing evidence that ear-notching and tail-docking procedures are painful for piglets regardless of birth weight and age at processing. The ABW piglets processed on d 3 produced calls of the greatest frequencies (Hz). Since handling and processing procedures were not separated, it is unclear if differences in vocalizations are due to an age-dependent aversion to handling as was previously shown (Taylor et al., 2001; Torrey et al., 2009) or to an increased painfulness of the procedures at older ages. Overall, the observed differences in call rate and

Processing low-birth-weight piglets

call frequency (Hz) are thought to reflect differences in piglet vigor or, more specifically, the casual observance of decreased vitality in LBW piglets. Cutler et al. (1999) recognized the tendency for LBW piglets to be weaker, and although data were not presented in the current study, notable lethargy was observed casually for the majority of LBW piglets surviving to time of ear notching and tail docking. With regard to vocalizations, LBW piglets produced fewer low frequency calls than ABW conspecifics but a similar number of high frequency calls. It is therefore likely that the increased lethargy and decreased vigor of LBW piglets resulted in fewer total vocalizations, except in response to painful stimuli such as tail docking and ear notching, when their call frequency was comparable to that of ABW piglets. However, it is also plausible that for LBW piglets the increased proportion of high-frequency versus lowfrequency vocalizations reflects a physical constraint on acoustic features due to body size. Smaller animals, with shorter, tenser (and possibly thinner) vocal folds, produce vocalizations of greater frequency (Hz; Ey et al., 2007). It is therefore possible that LBW piglets are simply less capable of producing low-frequency sounds. Behavior Immediate Effects of Ear Notching and Tail Docking. There were several behavioral differences between the weight classes of piglets observed immediately following the processing procedure. The differences in lying and dog-sitting between ABW and LBW piglets may be attributed to experimental design. Indeed, for the 10 min observation period after the procedure, 3 piglets were placed in a plastic box with a heat lamp placed at one end. Due to the thermoregulatory preferences of each piglet and differences in activity between weight classes, LBW piglets often rose to a dog-sit to avoid being stepped on by the larger piglets while recumbent. It was noted that when general activity decreased, LBW piglets typically repositioned atop ABW littermates, thus accounting for the increased huddling behavior of (and initiated by) LBW piglets. Position and/or movement of the tail, such as wagging, have been used as a measure of piglet distress following the tail docking procedure (Noonan et al., 1994; Sutherland et al., 2008). Tail wagging (rapid movement of the tail from side to side) occurred less often in LBW than ABW piglets although this may have been due to the lethargy of the LBW piglets. It has been theorized that since tail jamming (tucking the tail between the hind legs) occurs solely as a response to tail docking, it could be indicative of pain or discomfort (Noonan et al., 1994; Sutherland et al., 2008) although this has not been validated scientifically. Downloaded from https://academic.oup.com/jas/article-abstract/92/4/1718/4703441 by University of Adelaide user on 04 May 2018

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Effects on Suckling Behavior. Due to a lack of brown fat and immunoglobulins and very limited energy reserves (Herpin et al., 2002), piglets are dependent on colostrum consumption and the sow’s heat production immediately following farrowing for survival (Le Dividich et al., 2005). The average temperature difference between the intrauterine and external environment is 15 to 20°C (Herpin et al., 2002). For the piglet, this results in a 2°C drop in body temperature within 20 min postpartum, which is normally regained within the first 48 h (Herpin et al., 2002). In addition to the greater initial temperature losses due to increased surface area, the highly variable rate of thermogenesis for LBW piglets places them at a greater risk than ABW piglets of death from crushing, starvation, and disease (Herpin et al., 2002). Although external heat sources are typically provided in commercial production, piglets prefer the udder as a heat source during the critical rewarming period over the first 2 d postpartum. Current results are in accordance, with piglets on d 1 lying in close proximity to the sow even between nursing bouts. For both the postnatal and after-processing periods, LBW male piglets had the poorest attendance at nursing bouts and spent the greatest amount of time alone between nursing bouts, which may have impacted survivability if colostrum intake was affected (Nowak et al., 2000). Growth Rates and Mortalities The rate of ABW piglet mortality observed in the current study, 7.32%, is an improvement on the reported 10 to 13% range typically observed in industry (Herpin et al., 2002) and this was most likely due to attendance at all farrowings (Dewey et al., 2008). The 30.2% mortality rate of LBW piglets is similar to previous investigations on lightweight piglets (Marchant et al., 2000). It must also be considered that piglets weighing less than 0.6 kg were excluded from the study given their markedly low survivability (Dewey et al., 2008). A statistical tendency existed for increased preweaning mortality of piglets processed on d 1 although age was a confounding effect since it has been estimated that the majority of preweaning mortalities occur within the first 36 h after birth (Cutler et al., 1999). Mortality rate was considerably greater for male piglets in our study corroborating results of Lay et al. (2002), who speculated that this effect could be related to increased basal cortisol concentrations in male piglets (Ruis et al., 1997), in turn making them more susceptible to stress and disease, or to a greater sensitivity to maternal pheromones, which may draw the male piglets closer to the udder, thereby placing them at greater risk for crushing by the sow. Male piglets were also found to have an increased latency to suckle at birth, which Bate et al. (1985) attributed to el-

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evated testosterone concentrations. However, this was not likely an important factor in the current study because all experimental piglets were placed on the udder at the same time. The impaired thermogenic capacity of LBW piglets (Herpin et al., 2002) combined with the increased solitary behavior of male LBW piglets substantiates their increased mortality rate. Supplemental care was not provided to any of the piglets in this study although it is possible that “maximal care” (as described by Dewey et al., 2008) may have increased survivability for LBW piglets. Overall, the odds of a LBW piglet surviving to weaning were 5.5 times lower than for an ABW piglet in the current study. Although measurements stopped at weaning, LBW piglets often exhibit low postweaning survivability and poor growth performance (Quiniou et al., 2002; Smith et al., 2007). Of the surviving LBW piglets, growth performance through to weaning was reduced compared with ABW counterparts. Insulin-Like Growth Factor-I Concentrations and Immune Measures Concentrations of IGF-I, IgA, and IgG were measured as general determinants of colostrum intake and passive transfer of immunity. Mean IGF-I concentrations were lower than our previous findings for newborn piglet plasma (Torrey et al., 2009) but similar to concentrations in poor-growing 30-d-old piglets (Saleri et al., 2001). Concentrations of other immune measures were consistent with the literature: serum IgA (Torrey et al., 2009), serum IgG (Bland et al., 2003; Martin et al., 2005), and colostral IgA (Torrey et al., 2009) and IgG (Devillers et al., 2007). For LBW piglets, the lower IGF-I and serum IgG and the tendency for lower serum IgA in LBW compared with ABW piglets show that LBW piglets either consumed less colostrum or had a reduced transfer of immunoglobulins than ABW piglets. However, the values for LBW piglets fall within ranges previously reported (Bland et al., 2003; Martin et al., 2005; Torrey et al., 2009), so the statistical differences between weight classes may not be of biological significance. Immunoglobulin transfer is mainly dependant on colostrum intake, which is related to birth weight and immunoglobulin concentration in colostrum (Devillers et al., 2011). Therefore, placing experimental piglets all at the same time at the udder prevented the effect of birth rank and favored an optimal colostrum intake, which would be sufficient for a good immune transfer. Additionally, the lack of effects of age at processing or weight class × age at processing suggest that the procedures of ear notching and tail docking are of equal consequence on the acquisition of immunoglobulins by piglets of LBW or ABW, whether performed at 1 or 3 d of age. This is consistent with our previous findings Downloaded from https://academic.oup.com/jas/article-abstract/92/4/1718/4703441 by University of Adelaide user on 04 May 2018

(Torrey et al., 2009) showing no difference in immunoglobulin concentrations in ABW piglets tail docked and ear notched at 1 or 3 d of age. Conclusions In conclusion, tail docking and ear notching, 2 procedures that may be performed as part of routine piglet processing in North America, appear to be equally painful and distressing to piglets of LBW or ABW. Despite results from our study showing equivocal effects of processing at either 1 or 3 d of age on suckling behavior, growth, and measures of colostrally derived growth factors and immunoglobulins, vocalization data suggest that ABW piglets may be less reactive to the procedures on d 1 than on d 3. Additionally, given the decreased likelihood of a LBW piglet surviving to weaning and the fact that LBW piglets weighed significantly less at weaning than ABW piglets, delaying processing for LBW piglets may eliminate unnecessary procedures. LITERATURE CITED Bate, L. A., M. B. Kreukniet, and R. R. Hacker. 1985. The relationship between serum testosterone levels, sex, and teat-seeking ability of newborn piglets. Can. J. Anim. Sci. 65:627–630. Bland, I. M., J. A. Rooke, V. C. Bland, A. G. Sinclair, and S. A. Edwards. 2003. Appearance of immunoglobulin G in the plasma of piglets following intake of colostrum, with or without a delay in sucking. Anim. Sci. 77:277–286. Cutler, R. S., V. A. Fahy, G. M. Cronin, and E. M. Spicer. 1999. Preweaning mortality. In: B. E. Straw, J. J. Zimmerman, S. D’Allaire, and D. J. Taylor, editors, Diseases of swine. 9th ed. Blackwell Publishing, Ames, IA. p. 985–1002. Devillers, N., C. Farmer, J. Le Dividich, and A. Prunier. 2007. Variability of colostrum yield and colostrum intake in pigs. Animal 1:1033–1041. Devillers, N., J. Le Dividich, and A. Prunier. 2011. Influence of colostrum intake on piglet survival and immunity. Animal 5(10):1605–1612. Dewey, C. E., T. Gomes, and K. Richardson. 2008. Field trial to determine the impact of providing additional care to litters on weaning weights of pigs. Can. J. Vet. Res. 72:390–395. Ey, E., D. Pfefferle, and J. Fischer. 2007. Do age- and sex-related variations reliably reflect body size in non-human primate vocalizations? A review. Primates 48:253–267. Fraser, D. 1980. A review of the behavioural mechanism of milk ejection of the domestic pig. Appl. Anim. Ethol. 6:247–255. Hay, M., A. Vulin, S. Genin, P. Sales, and A. Prunier. 2003. Assessment of pain induced by castration in piglets: Behavioural and physiological responses over the subsequent 5 days. Appl. Anim. Behav. Sci. 82:201–218. Herpin, P., M. Damon, and J. Le Dividich. 2002. Development of thermoregulation and neonatal survival in pigs. Livest. Prod. Sci. 78:25–45. Kramer, M. S., F. H. McLean, M. Olivier, D. M. Willis, and R. H. Usher. 1989. Body proportionality and head and length ‘sparing’ in growthretarded neonates: a critical reappraisal. Pediatrics. 84:717-723. Lay, D. C., Jr., R. L. Matteri, J. A. Carroll, T. J. Fangman, and T. J. Safranski. 2002. Preweaning survival in swine. J. Anim. Sci. 80:74–86.

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