Introduction

Approximately 85 % of the world’s domestic South American camelids (SAC) are in Peru. This represents more than 5 million animals of which 4 million are alpacas (Vicugna pacos) and 1.2 million are llamas (Lama glama)¹. Raising SAC is the principal means of subsistence in the Peruvian Andean highlands since it is sustainable in this environment and provides wool and meat^2-5. Slaughter weight for alpacas is approximately 50 kg (52 % carcass yield) and for llamas it is 63 kg (55 % carcass yield)^2,6.

Animal welfare (AW) is defined as the overall mental and physical health condition in which the animal is in harmony with its environment⁷. This condition is ethically and commercially important and aimed at reducing detrimental stress, or distress, and preventing injury to animals during breeding, handling and transport^8,9. Transport of animals to the slaughterhouse can be a stress factor, and its effect increases with elapsed time^10,11,12. Such is its potential effect on AW that the World Organization of Animal Health (OIE) provides parameters and regulations for terrestrial transport of animals (Terrestrial Animal Health Code)¹³.

Distress causes elevation of catecholamine and blood cortisol levels^14,15, and consequent consumption of muscular and hepatic glycogen, affecting lactic acid formation and lowering muscle pH¹⁶. Levels of pH greater than 5.8 cause the dark-firm-dry (DFD) phenomenon in meat¹⁷. Lesions on carcasses lower meat quality, and require additional dressing of the injured parts, which affects final meat sale price¹⁰. Despite its importance, no research has been done to date on the well-being of SAC during transport to slaughterhouses. In contrast, this aspect of cattle raising has been extensively studied; for example, in one study 58 % of bovine carcasses exhibited evidence of abuse during animal loading, handling and transport to the slaughterhouse¹⁰. The present study objective was to document handling practices used with South American camelids during transport to slaughter, and evaluate them considering animal welfare criteria, using post-slaughter carcass lesions as an indicator of mistreatment.

Material and methods

Data were collected at the Huancavelica municipal slaughterhouse, Huancavelica Department, Peru. A total of 203 SAC carcasses were evaluated and information gathered on transport methods.

Description of animal transport to the slaughterhouse was done using a survey validated by an AW group in Argentina. Information on transport time was collected in terms of hours to the slaughterhouse, kilometers traversed and road characteristics (trail, pavement, dirt and mixed). Handling information included type of fastening (i.e. if ropes were tied to anterior extremities, posterior extremities or both), vision restriction, sex, total number of animals transported per vehicle type, and means of transport (by vehicle or on foot). Vehicle types were four-passenger car, pick-up truck, cargo truck, passenger bus or minibus. Data was also recorded on what part of a vehicle the animals were transported in; for example, in the cabin (with and without passengers), the bed, the roof and even in the trunk. Animal density per vehicle could not be calculated due to wide variation in vehicle characteristics. When animals arrived at the slaughterhouse it was observed if they had fallen or died. Unloading was described in terms of wait time pre-unloading, during unloading and pre-slaughter, and if it rained. Handler behavior was also recorded from unloading to the rest corral. Observations were taken of if the animals were pulled by the ears, grabbed by the fleece in lateral areas of the thorax and abdomen, if shouts or whistles were used, and if they were lifted by the rump or beaten in this area.

Carcass lesions were documented by an evaluator on the slaughter floor immediately after slaughter. They were described by direct observation and classified by depth as Grade 1 (superficial, involving subcutaneous tissue and outermost portion of muscle), Grade 2 (intermediate, muscle damage), and Grade 3 (deep, all tissue levels affected, including bone). Lesion area was classified as type A (< 25 cm²), B (25 to 100 cm²), C (> 100 cm²), and generalized (when injury covered at least one entire body region). Affected carcass area was indicated as Region 1 (pelvic area), Region 2 (thorax and abdomen) and Region 3 (lateral surface of thorax, cervical vertebrae and first five thoracic vertebrae).

Data were processed with the Infostat/E ver. 2015e statistical package using a 95% confidence level and 80+% power^10,18. Analysis was done with parametric and non-parametric descriptive statistics. A chi-squared test was applied to identify associations between handling and transport characteristics and the presence of lesions on the carcasses. The odds ratio (OR) was calculated using PROC LOGISTIC in the Statistical Analysis Systems, version 9.1.3 program (SAS Institute Inc., Cary, NC, USA). The study design was approved by the Institutional Animal Ethics Committee of the Cayetano Heredia Peruvian University (CONS-CIEA-054-2015).

Results

Most (64.6 %) of the SAC transported to the evaluated slaughterhouse were male. A total of 1,418 lesions were identified on all the carcasses with an average of 6.9 ± 0.2 per carcass.

Carcass lesions

A total of 1,418 lesions were documented during the slaughter floor inspection. Most were Grade 1 depth (74.0 %), Type A in area (65.5 %), and almost half (48.8 %) were located in Region 2 (Table 2).

Table 2 Carcass lesion distribution: depth, area and location (N = 203) 

Lesion characteristic	n	%
Depth:
Degree 1	1049	74.0
Degree 2	368	25.9
Degree 3	1	0.1
Area:
Type A	932	65.5
Type B	264	18.6
Type C	222	15.6
General	4	0.3
Location:
Region 1	421	29.7
Region 2	692	48.8
Region 3	305	21.5

Download time was less than 10 min in most (77.8 %) transport methods, and wrangling method was largely mixed (48.1 %), employing yells, objects, blows and slaps, among others, to drive the animals. Pre-slaughter rest time was 24 h in 70 % of the groups. Rain during unloading was observed in 21 of the 27 groups arriving at the slaughterhouse. Road type as reported by carriers was trail or path in 44.4 % of cases. Neither rain nor road type constituted risk factors for carcass lesions.

Transport in vehicles more than doubled (OR= 2.20; CI 95%: 1.27-3.82) the probability of Grade 2 and 3 lesions compared to transport on foot, but had no effect on lesion area (Figure 1). Non-restriction of vision also substantially increased the risk of large area (type C) lesions (OR = 2.26; CI 95%: 1.66-3.06), as did a pre-slaughter wait time longer than 24 h (OR = 1.42; CI 95%: 0.99 - 2.03) (Table 3).

Figure 1 Putative cause/effect relationships for transport-related lesions in South American camelids 

Table 3 Factors associated with lesions in South American camelids by area and degree 

	Area		Degree
	OR	CI 95%	OR	CI 95%
Vehicle type	2.20	1.27 - 3.82	0.86	0.61 - 1.22
Vision restricted	1.19	0.86 - 1.65	2.28	1.67 - 3.11
Rest time	1.42	0.99 - 2.03	1.13	0.85 - 1.5

OR = odds ratio.

Discussion

Presence of at least one injury in the post-slaughter inspections in the present results indicates overall poor animal management practices. This coincides with a previous report in which 92 % of the 264 studied carcasses exhibited at least one lesion with an average of 3.5 lesions per animal¹⁹.

Animal handling and transport are the most stressful and dangerous stages in the livestock production chain^{(5, 20,21)}. The present data confirm this in that the highest average lesion rates were in animals that had been transported in trucks (85.5 %) and minibuses (83.5 %). Abusive handling practices were also documented such as blows with fists and feet, stepping on the animal, as well as blows with wooden sticks, ropes, whips and rocks, among other stressful treatment (Table 1).

Restricting vision with a dark band is known to have a calming effect on livestock²². This agrees with the present results which indicate that animals transported with restricted vision remained calmer during transport and consequently experienced fewer injuries. In contrast to cattle²³, rain did not represent a risk factor for lesions among the evaluated SAC. This may be due to the digital pads of SAC, which allows them to better adhere to surfaces.

Pre-slaughter rest time exceeded 24 h in 70 % of the transported animals. This poses a risk for extensive injuries since they can become aggressive when different groups are mixed in the same corral and they begin to establish hierarchies. Some of the recorded lesions could have resulted from fighting during rest time. The present results agree with previous reports^17,24,25 in that the most frequent lesions are Grade 1, followed by Grade 2 and a very few Grade 3.

Distribution of pre-slaughter lesions in cattle is dominated by small area (2 to 8 cm diameter), and Grade 1 lesions (subcutaneous tissue) largely on the legs, iliac crest and abdomen. Larger, deeper lesions occur mostly in the loin, shoulder and thorax regions¹⁹. The lesion distribution observed here in SAC differs from the pattern in cattle in that 48% of the lesions were located between the thorax and the abdomen. A number of factors may contribute to this pattern, such as scant adipose tissue coverage, the minimal space provided animals during transport, and inappropriate design of transport vehicles. These factors can facilitate blows and traumas against the surface, walls and floor of the transport space, negatively affecting AW. Another possible factor is the use of ropes tied around the posterior portion of the animal, surrounding the caudal part of the abdomen and cranial region of the rump. Injuries occur when the animals attempt to stand, causing the ropes to scrape them and resulting in extensive surface damage. During transport the animals also bump into each, and hit the walls and/or floor. Inadequate restraints frequently cause unnecessary stress to the animals, as well as injury from the restraining method.

Guidelines do exist for camelid transport in terms of the proper use of transport method, vehicle size and number of animals to be loaded^{(26, 27,28)}. In Peru the SENASA publishes a guide to best livestock practices²⁹, but it includes no specific mention of SAC. Preferable conditions for SAC transport include sufficient space to keep animals calm during transport, as well as providing food and water during long periods of transport, as recommended by the OIE²⁶. Only trucks can provide enough space for maintaining SAC well-being and comfort during transport, considering that a load density of 0.55 m² is required for an adult alpaca (40 to 55 kg body weight)⁵.