This study proposed new ABMs for camels and evaluated their associations with resource and management-related factors in dromedary camels kept in a permanent market. Our methodological approach, although did not presume to define direct cause-effect relationships, could verify the validity of some ABMs as welfare indicators as well as identify relevant factors related to housing and management that were likely linked to camel welfare. Thus, our findings may be useful to recognize welfare issues and propose guidelines to safeguard welfare in camels kept in intensive systems.
The space allowance and the number of camels per pen stood out among the management factors affecting camel welfare, being associated with many of the proposed ABMs. In pens where space allowance was less than 19 m2 per animal, indeed, camels had the worse Thirst index as well as the highest likelihood of showing pain induced by management procedures and aggressive behaviours. These associations may be linked to both logistic and social factors. First, water and feed supply in overcrowded pens are more demanding from a management point of view, and besides, require facility adjustments. The probability, therefore, that water and feed needs are not fulfilled in overcrowded pens could be greater. Second, camels in overcrowded pens have limited opportunity to walk freely and frequently experience unstable social relationships. In this context, natural behaviours are inhibited (Wang et al., 2016) and dynamic dominance hierarchies characterized by high levels of agonistic behaviours could increase (Fu et al., 2016; Eriksson et al., 2021). Under natural conditions, indeed, camels move over very large areas and are great walkers, practising “ambulatory grazing” (Faye, 2020). Camels, moreover, are herd animals but groups are, in general, stable and not large. They indeed comprised around 9 animals including one adult bull, adult females, sub-adults, and young (Wilson, 1990; Schulte and Klingel, 1991). The risk of not meeting these ethological needs in intensive systems and livestock markets increases dramatically and, therefore, preventive measures are necessary. Our results indicated that a minimum space allowance of 19 m2 per camel could reduce the hazard of the negative welfare consequences. Caretakers, furthermore, should avoid the formation of too numerous herds, paying attention to their composition in terms of age, sex, and relationships between members in order to limit competitive hierarchies and negative social interactions. The effect of space allowance on camels’ welfare has been recently also evaluated by El Shoukary et al. (2020) and Zappaterra et al. (2021). Those authors showed that overcrowding had negative effects not only on behavior, increasing aggressions and stereotypies, but also on body conditions and reproductive performance of camels. Overcrowding is a recognized welfare concern for all the animals reared under intensive conditions (Nordquist et al., 2017). The adverse effect of limited space allowance on drinking and feeding behaviour, abnormal behaviours, and body lesions have been indeed shown in most livestock species (Salak-Johnson et al., 2012; Fu et al., 2016; Raspa et al., 2020; Eriksson et al., 2021).
Shaded space allowance was also associated with several proposed ABMs. Its link with the welfare criteria of absence of prolonged thirst, as evaluated by Thirst Index, is quite intuitive. However, our findings also showed that an ample shaded area was also associated with a reduction in the use of management procedures inducing pain (e.g. hobbles and nosering) and an improvement in the human-animal relationship. These findings may suggest that the presence of shade increased not only the thermal but also the social comfort of camels. It has recently been shown that camels have a preference for shade and express more behaviours indicating a quiet and positive state, such as recumbency and ruminating, in the shaded than sunny areas (Zappaterra et al., 2021). The opportunity to have positive experiences and express natural behaviours could have influenced their intra- and interspecies relationships resulting in an improvement of welfare outcomes. Moreover, if the shaded space is adequate for rearing density, camels could reduce competitive behaviour and peacefully share this resource. Our results seem also to support Mellor's concept, which emphasizes the role of positive experiences in the animal welfare assessment (Mellor, 2016). According to Mellor, welfare cannot be only defined on the basis of the animals’ responses to living in poor environments. It is also necessary to evaluate their opportunities to engage in behaviours they find rewarding, including thermal comfort, positive social interactions, resting and feeding behaviours (Mellor, 2016). Behavioural changes related to the presence of shaded areas have been shown both in intensive and extensive systems in several species, such as cattle, sheep, buffaloes, and horses, although previous studies mostly focused on the effect on productive traits (Schütz et al., 2010; Holcomb et al., 2015; Giro et al., 2019; De et al., 2020; Mishra, 2021). Our finding suggested that a shaded area of at least 7 m2 per animal (our ample category) had beneficial effects on several aspects of the camel's welfare but further studies should define specific recommendations according to the environmental heat load.
Bedding may affect animal welfare (Welfare Quality, 2009; AWIN, 2015). In our study, it was indeed associated with ABMs of Good feeding, Good housing, and Good health. It is interesting to note that camels having a disease were about 3 times more likely to live in pens with dirty bedding confirming that keeping bedding clean is a good practice that should be recommended to prevent diseases also in camels (Schwartz and Dioli, 1992). The role of bedding management on animal welfare has already been emphasized in other species such as cattle and horses (Quigley et al., 2017; Siegers et al., 2018; Robles et al., 2020). However, the magnitude of welfare consequences for camels could be very affected by climatic conditions. Their faeces may indeed dry out quickly in the arid climate where they are usually raised (Padalino and Menchetti, 2021). Further studies, with longitudinal designs and in differentiated settings, could better define the role of bedding quality for camel welfare and validate additional indicators, possibly animal-based, to evaluate farm hygienic conditions. For instance, a score rating the cleanliness of some anatomical regions of camels (e.g. udder, legs, and flanks) rather than the bedding could be a more useful and direct welfare indicator. This type of score has already been proposed as welfare indicators for cattle resulting associated with several productive and pathological parameters such as milk somatic cell counts, mastitis, and enteritis (Faye and Barnouin, 1985; Ellis et al., 2007; Wolf et al., 2016; Molina et al., 2019).
Measures related to feeding and water management were other factors linked to many ABMs. In some cases, the link between these management factors and the ABMs was expected and easy to explain. Ample feeding and water spaces were, for example, associated with good body conditions and the absence of thirst. It is indeed logical to expect an increase in feeding and drinking activity as available spaces increase, particularly for those subordinate camels that may have more difficulty accessing resources due to their low social rank (Turner et al., 2000; DeVries et al., 2004). Ample feeding and water spaces were also associated with reduced risk of pain induced by management procedures and improved camel behaviour. This finding confirms that increasing space allowance at the feed and water places could reduce competition and aggressive interactions among camels. As widely demonstrated in other species (Turner et al., 2000; DeVries et al., 2004), indeed, competition for resources is a primary reason for aggressive interactions in animals reared in groups under intensive systems. Sometimes, however, the relationship between management factors and ABMs could be less easy to explain. A management factor could just be a mediator or a confounder for other exposure variables; otherwise different factors may interact to produce different animal-based responses (EFSA, 2012c). We could also hypothesize that the behaviour of camels indirectly benefited from ample feeding and water spaces being mediated by the general improvement in body conditions. It has been shown, for example, that donkeys with a high BCS are friendlier with humans (Farhat et al., 2020). This hypothesis also supports the multidimensional concept of welfare in which biological functions, as indicated by BCS and Thirst Index, and affective state, as indicated by the absence of pain or fear, are connected and superimposed (Fraser, 2003). A feeding space >1.10 m2/camel and a water space >0.160 m2/camel may be suggested to obtain good welfare outcomes related to principles of Good feeding and health as well as of Appropriate behaviours. However, these thresholds were calculated based on our study population and require external validation (Menchetti et al., 2021).
Ad libitum distribution of water and the placement of the water points in the shade are good husbandry practices (Pritchard et al., 2005; Bergin and Nijman, 2019; Rodrigues et al., 2020). However, they were poorly followed in the market. The distribution of water was indeed rationed in about half of the pens and, for the most part, the water points were positioned in the sun. These factors were negatively associated with ABMs not only of Good housing but also of Good health. Water management is a well-known welfare issue for animals kept in several intensive and extensive contexts (Pritchard et al., 2005; Bergin and Nijman, 2019; Bekele et al., 2020; Rodrigues et al., 2020), but it may seem to be surprising for the camel due to its famous adaptability to resources scarcity. Thus, it is worthwhile noting that the odds of having a disease was 2 times higher in camels receiving rationed than ad libitum water suggesting that water supply is an aspect of camel welfare that cannot be overlooked (Menchetti et al., 2021; Padalino and Menchetti, 2021). It must also be taken into account that water needs in intensive systems are greater than in Bedouin ones (about 9 times higher to produce 1 litre of milk (Faye, 2013)). Our analyses also showed an inverse association between thirst and water temperature. In other words, non-thirsty camels were more likely to have hot water. This result was not expected and we can only speculate that the non-thirsty camels received water in overabundance and the excess water remaining in the trough increased its temperature over time. It, therefore, seems that the importance of having fresh water plays a secondary role compared to the benefits of ad libitum access.
Caretaker’s experience and productive purpose of the camel resulted associated with the proposed ABMs. In particular, a long experience of caretakers seemed to be a protective factor for disease and injuries. This was expected since it has been already reported that the health of camels could benefit from staff training (Menchetti et al., 2021). Regarding the productive purpose of camels, we curiously found that camels reared for milk or breeding were more likely to show signs of restricted movements than camels intended for slaughter. Perhaps the use of hobbles or ropes was more frequent in camel reared for milk or breeding as they needed to be more frequently moved and handled notably at milking time. The positive association between the presence of hobbles and ABMs such as pain or injuries is also worth mentioning to highlight the role of the limited freedom of movement and practices used for restraint on camel welfare. Limited freedom of movement has been already indicated as a factor that may have negative consequences from a social and metabolic point of view while the use of restraint tools is a direct cause of injuries, infections, and inflammations (Rayner et al., 2018; Farhat et al., 2020; Menchetti et al., 2021; Padalino and Menchetti, 2021). Therefore, when hobbles are considered unavoidable, it would be desirable to limit the use of inappropriate ropes, adopting also pain relief strategies, such as pads under the hobbles. Moreover, the camel's health status of camels wearing hobbles should be strictly monitored.
Finally, it is worth noting that the age of the camel was included in the applied statistical models as a covariate since it influenced several ABMs. For example, BCS increased as the camel’s age increases, probably due to age-related changes in body composition (Kenyon et al., 2014; Ouchene-Khelifi and Ouchene, 2021). As expected, the likelihood of having injuries also increased with increasing camel’s age while it appeared that aggressive behavioural responses to the human approach reduced over time. The accumulated familiarity with human contact and the taming could explain this last result (Waiblinger et al., 2006). The human-animal relationship could be indeed influenced by several factors but many of these are linked to the quality of past experiences. Habituation and early positive human contacts as well as the use of positive reinforcements are husbandry practices that could improve animal´s perception of humans (Mota-Rojas et al., 2020) and should therefore be encouraged on camel farms. About a quarter of the camels at the market evaluated by the Approaching test showed negative responses to human contact. Farm animals showing human-direct aggression and problematic to handle not only may lose their commercial value and be repeatedly sold but could also be manipulated with techniques that can exacerbate the undesirable behaviours causing injuries and stress. Aggressive animals could eventually be suppressed (Burattini et al., 2020). Conversely, a good human-animal relationship has positive effects not only on the welfare of the animal but also on its productivity and product quality (Waiblinger et al., 2006; Mota-Rojas et al., 2020). Despite this key role in animal welfare (Waiblinger et al., 2006; Welfare Quality, 2009; EFSA, 2012c), the human-animal relationship is complicated to assess and cannot be measured directly (Waiblinger et al., 2006). It probably deserves more valorization in the camel protocol and the validation of additional ABMs for its assessment (Padalino and Menchetti, 2021).
Our findings need to be interpreted with caution due to several limitations of the study. The main limitations are probably linked to the cross-sectional approach. For example, our study did not take into account the magnitude of welfare consequences (duration x intensity (EFSA, 2012c)) and could not provide definite information about cause-and-effect relationships. As suggested by EFSA, the duration of the welfare consequences might not even be considered in risk analysis whether the applied welfare measures reflect a momentary situation (EFSA, 2012a). A major criticism could be to treat the duration of management factors as constant. Camels could indeed be frequently moved or sold and this made the exposure to management factors very dynamic. Moreover, the quantitative indications concerning for example space allowance cannot be generalized, because these numbers were strictly related to our study population and require external validations as well as adjustments based on the type of scenario. It is also worth highlighting that among the categorical variables, the ABMs related to presence of a disease were limited by the type of assessments, which allows only to record the presence of major clinical signs. This could be overcame probably including more specific ABMs, able to identify the type of disease according to their original causes, and including longitudinal evaluations. As suggested by Faye et al. (1999), diseases can be classified into "immanent diseases", linked to the practices and conditions of the farms, and "transcendental diseases", coming from external causes (affecting all farming system independently of the practices and local environments, such as cases of Rift Valley Fever, MERS-Cov, anthrax, rabies, and brucellosis). This approach would clarify better the implications of the disease on camel welfare and how to prevent it. Finally, validation of the selected ABMs would require repeated measurements and the involvement of other researchers (EFSA, 2012c). Monitoring and surveillance systems inside the camels' pens/farms as well as a broad application of the welfare assessment protocol will help fill these gaps. Despite these limitations, the approach chosen in the selection of both animal-based and management-based measures complied with the feasibility features required for an on-farm welfare assessment (Main et al., 2007; EFSA, 2012a). These measures, moreover, seem “fit for purpose” (EFSA, 2012c) as identified several plausible welfare consequences as well as practicable corrective actions.
Overall, this study proposed new practical and feasible ABMs for dromedary camels kept under intensive management. They seemed to be appropriate indicators of welfare consequences in this species being able to identify factors related to housing and management practices that may impair or improve camel welfare. Our preliminary results need to be validated on a larger dataset, but they may be the first steps towards the development of welfare standards and guidelines for dromedary camels.