Animal (2020), 14:4, pp 667–669 © The Author(s) 2020. This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited. animal doi:10.1017/S1751731119003306 Opinion paper: Measuring livestock robustness and resilience: are we on the right track? P. Llonch1† , G. Hoffmann2, R. Bodas3, D. Mirbach4, C. Verwer5 and M. J. Haskell6 1 Department of Animal and Food Science, Universitat Autònoma de Barcelona, Travessera dels Turons S/N, 08193 Cerdanyola del Vallès, Spain; 2Department of Engineering for Livestock Management, Leibniz Institute for Agricultural Engineering and Bioeconomy, Max-Eyth-Allee 100, 14469 Potsdam, Germany; 3Instituto de Ganadería de Montaña, Consejo Superior de Investigaciones Científicas–Universidad de León, Finca Zamadueñas, Ctra. Burgos km 119, 47071 Valladolid, Spain; 4 Deutsche Landwirtschafts-Gesellschaft e.V. – German Agricultural Society, Eschborner Landstrasse 122, 60489 Frankfurt/Main, Germany; 5Louis Bolk Institute, Kosterijland 3-5, 3981 AJ Bunnik, The Netherlands; 6Animal & Veterinary Sciences Research Group, Scotland’s Rural College (SRUC), King's Building - West Mains Road, EH9 3JG Edinburgh, UK Introduction can apply not only to individual animals but also to higher organisational levels such as at the farm or system level. Animal production is a cornerstone of employment and social It refers to the adaptive capacity of a complex system to cope structures in rural areas and, in some cases, it is highly with disturbances and, at the same time, maintain its functions. dependent on the environment, which in a context of climate change makes it very vulnerable. For animal production sys- tems to remain sustainable, this challenge must be managed Are robustness and resilience multidimensional or to achieve economic stability and good welfare. The terms trait specific? ‘robustness’ and ‘resilience’ are often used to describe a state of relative stability when animal production is confronted Robustness and resilience are often referred to as general against global warming. However, the assessment of robust- characteristics of animals. Whereas this is applicable to ness and resilience in animal production systems has some robustness (Friggens et al., 2017), resilience may be more gaps that need to be addressed prior to any definition specific to the type of stressor. For instance, it is possible that of strategies to improve them. The methods to assess robust- a cow that copes well with heat as a stressor may not man- ness and resilience have to be specific and provide a com- age so well with certain diseases. An example is the ‘slick’ prehensive and dynamic assessment. This opinion paper hair gene that confers a degree of heat resistance for animals introduces these needs and suggests some potential solu- carrying that gene (Olson et al., 2003), but it is not known tions to tackle them, using dairy production as example as (but not expected) that this gene will confer any resistance it is one of the animal production systems most exposed to infectious disease, as the characteristics that confer resil- to forecasted environmental changes endangering feed ience to independent traits may not necessarily related to scarcity, emergence of new diseases and increased heat stress. each other. Therefore, resilience is not considered to be a general trait in the sense that cows, or systems, are not more or less resilient but this has to be assessed for each particular Robustness and resilience: all about adaptation trait. On the other hand, robustness may provide information capacity about the individual animal or the system, which facilitates comparisons, based on multiple components including the Robustness and resilience have been sometimes used analo- resilience to each challenge. Considering this, robustness gously. However, these two terms refer to different concepts. should be measured as a multidimensional attribute affecting Resilience is the ability of an animal to adapt to stressors and either the whole animal or system, making comparisons its ability to return to the ‘normal’ state (Urruty et al., 2016). between individuals or systems more plausible than resil- Robustness, though, is the ability to express a high produc- ience, as what is measured is the outcome rather than the tion potential combined with resilience to stressors in a wide relative response. variety of environmental conditions without compromising reproduction, health and welfare (Colditz and Hine, 2016). In short, robustness implies that the animal maintains Comprehensive assessment of robustness functionality when a stressor is applied, which inevitably and resilience includes resilience. Both concepts, robustness and resilience, Resilience can be assessed through the strategies triggered † E-mail: pol.llonch@uab.cat by the organism to cope with an environmental challenge 667 Llonch, Hoffmann, Bodas, Mirbach, Verwer and Haskell (e.g. behaviour) and the consequences on the challenged might maintain good foot health (e.g. regular foot-bathing, organism (e.g. milk yield and quality). The coping strategies good flooring, good cleanliness) and Farm ‘B’ has poor consist of the effort made by the animal to cope with the conditions (no foot-care, cracked concrete, not cleaned). challenge, which can not only be behavioural, metabolic, On Farm ‘A’, the cows mostly have good feet and low lame- physiological changes in the short term but can also result ness scores. Can we say that they are resilient in terms of in morphological changes in the longer term. For instance, lameness? Strictly speaking, we cannot, because we have an animal challenged by heat can react rapidly by seeking not seen them challenged. On Farm ‘B’, we see cows that shade, reducing metabolic energy expenditure and panting are lame and some that are not lame. We might conclude to cope with heat stress in the short term, whereas a longer that non-lame cows are robust, because they have main- term reaction could reduce the hair density on their skin. tained functionality in a challenging situation, whereas lame The consequences may vary among individuals not only cows are not. In order to assess the degree of robustness and in the magnitude of the response but also in the type of resilience in individual animals or systems, we need to consequence. For instance, two cows exposed to heat stress observe their adaptive response to changes in the environ- will react differently, triggering different mechanisms to cope ment, assessing them in good conditions and contrast this with the stressor. One cow might reduce feed intake to against the response to the challenge. reduce heat production during rumen fermentation, whereas To assess the ability of an animal to respond and recover the other cow might reduce activity to decrease heat produc- from challenge, some parameters are needed that can be mea- tion from the skeletal muscles. Both strategies pursue the sured easily, have been accurately validated, can be objectively same goal, which is to reduce body temperature, but using assessed and ideally measured at any time point. Research different mechanisms. The consequences inform about the studies have identified a number of these phenotypic traits impact of the stressor to the organism irrespective of the on farms, slaughterhouses, etc. including behaviour, metabo- adopted mechanisms to adapt to the challenge. An example lism, physiology and anatomic characters. However, these of this would be the change in body temperature during heat phenotypic indicators have been typically used as ‘snapshot’ load. For a comprehensive assessment of the adaptive capac- measures, whereas to assess robustness and resilience mea- ity, both the coping strategies and the consequences should sures taken across the time course of a challenge are needed. be addressed as they are interrelated. An incomplete assess- The phenotype could be determined in experimental condi- ment of the adaptive capacity based either on one mitigation tions by challenging an individual with some form of stressor trait (say activity or feeding behaviour) or a single conse- and by subsequent longitudinal evaluation of various indica- quence could lead to inaccurate conclusions as it risks of tors over time. Along with research, data from commercial not reflecting the true coping cost for the animal. A refined farms could be a precious source of information about this determination of resilience should include a comprehensive adaptive capacity to unplanned perturbations. Currently avail- phenotyping balancing the most active strategies to cope able technology based on precision livestock farming offers an with a stressor against its consequences. Taking again the enormous potential to gather information about the changes example of heat stress, the resilience towards heat can only in the phenotype (both for adaptation strategies or conse- be assessed by contrasting the increase in body temperature quences) due to commercially relevant stressors. These data (i.e. the consequence) in relation to the strategies engaged in may be extremely beneficial for producers and policy makers its mitigations, such as changes in feeding behaviour, reduc- on the most adequate strategies to improve robustness and tion of metabolism and panting, to mention a few. resilience (Berghof et al., 2018), including breeding programmes and management actions. Longitudinal assessment of robustness and resilience Actions needed for a reliable assessment Challenges to animals and systems vary in type and length. A challenge such as heat stress is typically of shorter duration Integration of robustness into animal breeding programmes than of poor housing that might last the lifetime of a cow. will improve the capacity of animal production systems to In the definition of resilience discussed above, there is the tackle the forecasted global change. Improving robustness concept that the animal, farm or system has the ability to inevitably implies increasing resilience towards environmen- ‘bounce back’ from stressors, which is especially relevant tal challenges. To improve robustness and resilience, reliable when they are short term. However, as robustness describes methods to monitor them should be considered, which the capacity to withstand in harsh conditions, longer term will not be able to achieve unless a specific, comprehensive scenarios are needed to be able to measure it. Irrespective and longitudinal assessment is implemented. Specificity of the duration of the challenge, we must observe the animal means that only the relevant traits associated with the adap- or system before, during and after the period of challenge to tive response towards a thread should be considered. A com- allow us to see the magnitude and the duration of the prehensive assessment means that the biological response response. As an example, we could consider robustness in towards a challenge has to balance the main adaptation cow foot health. We can use a score to assess lameness in strategies carried out by the animal (e.g. panting) and the cows on two farms. Farm ‘A’ has very good conditions that consequences (e.g. body temperature) for the organism. 668 Measuring livestock robustness and resilience A longitudinal assessment implies that animals have to be necessarily reflect the views or policies of the EiP-AGRI neither in constant monitoring that is able to inform about the evo- the DG Agriculture of the European Union. lution of the response against the threat. Current precision P. Llonch 0000-0001-5958-861X livestock farming tools offer the possibility to provide the amount of data necessary to comply with these demands. Declaration of interest Progressive implementation of these tools in animal farming None. will inform farmers, breeding companies and policy makers about the hottest gaps that needs to be addressed to improve Ethics statement robustness and resilience in livestock systems. All ethical standards have been met. Acknowledgements Software and data repository resources In its effort to transfer the research achievements to the rural None. sector, the agricultural European Innovation Partnership (EiP-AGRI) from the Directorate General of Agriculture of the European Commission has promoted Focus Groups that References gathered experts on a specific area to discuss strategies Berghof T, Poppe M and Mulder H 2018. Opportunities to improve resilience in addressing current or emerging threats for Europe’s agriculture. animal breeding programs. Frontiers in Genetics 9, 692. The Focus Group Robust and Resilient Dairy Production Colditz IG and Hine BC 2016. Resilience in farm animals: biology, management, Systems focused on identifying the main threats for dairy pro- breeding and implications for animal welfare. Animal Production Science 56, 1961–1983. duction as well as suggesting the most promising and realistic Friggens NC, Blanc F, Berry DP and Puillet L 2017. Deciphering animal strategies to tackle them. Authors acknowledge the initiative of robustness. A synthesis to facilitate its use in livestock breeding and management. the EiP-AGRI, which gave the opportunity for discussions Animal 11, 2237–2251. that results in this opinion paper. We would also like to thank Olson TA, Lucena C, Chase CC Jr. and Hammond AC 2003. Evidence of a major José Pires (INRA) and the EiP-AGRI staff (Remco Schreuder, gene influencing hair length and heat tolerance in Bos Taurus. Journal of Animal Science 81, 80–90. Cesar Resch, Quico Onega and Sirpa Karjalainen) for their con- Urruty N, Tailliez-Lefebvre D and Huyghe C 2016. Stability, robustness, vulner- tributions during the discussion. The views expressed in this ability and resilience of agricultural systems. A review. Agronomy for Sustainable publication reflect the opinion of the authors but do not Development 36, 15. 669