Animal welfare outcomes

For an environmental enrichment to be effective it must improve animal welfare. The nature of the improvement may be complex due to, for example, potential animal welfare trade-offs (e.g. negative health impacts but improvements to positive affect — see section on risk below), and the method of welfare assessment. The optimal approach to assess animal welfare has been debated but it is now well accepted that there is not one single indicator of animal welfare and, hence, welfare is best assessed using a combination of indicators (Fraser et al. Reference Fraser, Weary, Pajor and Milligan1997; Duncan Reference Duncan2005; Fraser Reference Fraser2008; Hemsworth & Coleman Reference Hemsworth and Coleman2011). We consider short- and long-term effects and ask if the provision of a specific environmental enrichment reduces suffering (i.e. ‘enrichment for meeting basic needs’; evident by fewer injuries, less pre-clinical and clinical disease and normal biological functioning), and/or if the enrichment is something that the animal wants beyond basic needs (i.e. ‘enrichment for pleasure’; evident by preference, behavioural demand, long-term utilisation of enrichments and ‘enrichment for positive welfare balance’; long-term effects of positive experiences that outweigh negative welfare experiences, such as positive mood and stress resilience; Table 1). We refer to basic needs as both ultimate and proximal physiological and behavioural needs that when thwarted result in poor health, frustration or stress. The approach implies the nature of the improvements to animal welfare, whilst acknowledging that providing an animal with what it wants and likes can provide positive experiences even when not all of its basic needs are met (see Rault et al. Reference Rault, Hintze, Camerlink and Yee2020).

Table 1. Proposed re-classification of environmental enrichment provided to animals based on both short- and long-term assessments of welfare indicators

↑ Indicates improvement after the provision of enrichment.

↔ Indicates no improvement to welfare indicator after the provision of enrichment.

Pseudo-enrichment refers to proposed environmental enrichments that do not improve biological functioning, provide sustained pleasure or result in a positive welfare balance.

* This item may be beneficial if it is included in an enrichment programme or rotated throughout an animal’s life, however when provided in isolation does not improve the welfare of the animal.

Barren environments and resources that do not contain a specific resource that an animal needs, can lead to suffering. Suffering can disrupt biological functioning which will be evidenced by compromised fitness traits, such as increased morbidity and mortality or impaired growth/body condition and reproduction (Broom & Johnson Reference Broom and Johnson1993; Moberg Reference Moberg2000; Hemsworth & Coleman Reference Hemsworth and Coleman2011). When an animal is provided with an environmental enrichment that meets a need, the prolonged stress responses and subsequent impacts on health and biological functioning will improve (Fraser & Duncan Reference Fraser and Duncan1998). As such, this component of the framework asks the question, does the enrichment prevent, or ease, animal suffering? Inclusion of ‘easing’ of suffering into this component builds on the Newberry (Reference Newberry1995) definition of enrichment as ‘something provided to an animal that is biologically relevant and prevents suffering’ and supports continued improvements in animal welfare. Of note, here we focus on (relatively) short-term effects/assessments (days to weeks; Table 2) after the provision of an enrichment, not immediate acute stress responses (minutes to days) induced by environmental enrichment (i.e. some novel objects) or long-term assessments that improve welfare in the long-term, such as increased stress resilience (Zulkifli & Siegel Reference Zulkifli and Siegel2019).

Table 2. Proposed assessments for each proposed environmental enrichment (EE) classification using science-based indicators of animal welfare. Short-term refers to days, weeks or months depending on the species and long-term refers to the whole life or production cycle of the animal

In agreement with the statement that enrichment should improve welfare beyond the absence of suffering (Boissy et al. Reference Boissy, Manteuffel, Jensen, Moe, Spruijt and Keeling2007), the proposed framework also considers both short-term positive hedonic experiences and long-term accumulative effects of positive hedonic experiences that outweigh negative experiences (Table 1). This question provides insight into the positive experiences that environmental enrichment can provide. Whether an environmental enrichment is something that an animal wants can be determined by assessing preferences for enrichments, motivation to access specific enrichments (behavioural demand) and use/interaction with the environmental enrichment over time (Table 2). Evidence suggests that what an animal wants (i.e. a specific environmental enrichment, or chooses one environmental enrichment over another) reflects what an animal likes and the associated experience of positive affective state (emotions), such as pleasure when it is obtained (Fraser & Duncan Reference Fraser and Duncan1998; Fountain et al. Reference Fountain, Hazel, Ryan and Taylor2020; Mendl & Paul Reference Mendl and Paul2020). However, there are many factors that must be considered with assessing positive hedonistic experiences through motivation and preference, such that the choices animals make can change over time. For example, cattle prefer pasture rather than a feedlot environment in the evening but prefer a feedlot environment in the morning; preferences are related to lying and feeding behaviour, respectively (Lee et al. Reference Lee, Fisher, Colditz, Lea and Ferguson2013). Furthermore, animals may become habituated to an enrichment which would be indicated by a decline in environmental enrichment utilisation over time (Guy et al. Reference Guy, Meads, Shiel and Edwards2013). This suggests that preferences, motivations and utilisation of enrichments should be monitored over the entire time-frame of interest, i.e. the whole production cycle or for the period of time that the environmental enrichment is allocated. If habituation occurs, our framework suggests that this enrichment on its own is not effective, although it may be effective when combined or rotated with other environmental enrichment items in a programme designed to maintain animal interest and use throughout their lifespan. For example, rope, straw and wood on a chain is more effective at improving sow welfare when provided on a rotation compared to consistent and continuous access (Roy et al. Reference Roy, Lippens, Kyeiwaa, Seddon, Connor and Brown2019) and novel objects that are not biologically relevant when rotated can improve chicken welfare (Altan et al. Reference Altan, Seremet and Bayraktar2013).

Our proposed framework includes short- and long-term assessments of animal welfare after the provision of potential enrichment items or programmes to understand. This approach more fully elucidates the nature of the improvements to animal welfare which enables the type of enrichment to be categorised (Table 1). Our framework then considers each category of enrichment in the context of economics. We argue that capturing the nature of the improvement to welfare allows clearer links between improvements to animal welfare and economics and, subsequently, this approach will increase uptake by producers and provide clarity to consumers looking to make informed buying decisions.

Characteristics of animal welfare outcomes

A prologue to this component of the framework acknowledges that we do not propose that animals housed in environments provided with effective environmental enrichments that they want and/or need are living ‘beyond basic needs.’ Rather, we provide a framework that can be used in a variety of ‘standard’ environments (noting that what is considered to be ‘standard’ constantly changes and evolves) to determine the magnitude of change of animal welfare after an environmental enrichment item/programme is provided; either enriching an animal’s environment by reducing suffering (i.e. environmental enrichment for meeting basic needs), providing pleasure or improving overall balance of positive welfare. Although our framework could suggest that environmental enrichments that reduce suffering are a lower tier than environmental enrichments that provide pleasure, we do not suggest that one is more important than the other. This approach acknowledges that enrichments that reduce suffering in some present-day environments may not be beneficial in the future (i.e. if the quality of standard housing environments improve) but also provides an avenue to provide environmental enrichments that improve animal welfare without prescribing unobtainable criteria for producers (i.e. provision of pleasure even if basic housing does not meet all of the animal’s basic needs). Thus, the framework provides a fluid threshold to determine ‘enriched environments’ which promotes continual improvements to production animal welfare.

Pseudo-enrichment

Pseudo-enrichment is a term devised by Würbel and Garner (Reference Würbel and Garner2007) referring to enrichments that do not improve rodent welfare in research and laboratory captive environments. We apply this terminology to refer to proposed environmental enrichment items and programmes that do not improve physical health and biological functioning, nor is there evidence that the enrichment is wanted by the animal. Not only is the animal unable to engage in intrinsically valuable experiences but the environment is lacking specific opportunities that an animal needs, resulting in chronic stress. As such, any enrichment in this category must never be considered effective environmental enrichment.

Environmental enrichment for meeting basic needs

Environmental enrichment for meeting basic needs indicates that the enrichment provides something that improves biological functioning. Enrichments that improve basic needs (i.e. physical health or biological functioning) focus on the ease of suffering. As such, they may be prescribed as standards in legislation or eventually be included in ‘standard housing’ environments. Enrichments in this category may simply reduce boredom in a barren environment, rather than provide something specific that an animal wants and, therefore, the outcome on animal welfare may not be directly transferable across production systems, enterprises or other environments. We acknowledge that positive affective states are likely experienced when a basic need is met, however this category excludes any environmental enrichments that result in long-term benefits for positive welfare balance (i.e. stress resilience). Theoretically, this category of enrichment may be classified as environmental enrichment to reduce suffering however this terminology may be too emotive for producers, industry or consumers, and therefore may limit uptake and support. Depending on the standard baseline, environmental enrichments provided in this category may provide animals with ‘a life worth living’ according to the Farm Animal Welfare Committee (2009). Although, it must be noted that environmental enrichments are not the only method to provide an animal with ‘a life worth living’ or ‘a good life’ — we restrict our discussions to environmental enrichments here, for a broader perspective see Farm Animal Welfare Committee (2009).

Environmental enrichment for pleasure

Environmental enrichments for pleasure are environmental enrichment items or programmes that provide the animal with something that it wants but does not improve health or biological functioning (i.e. it is something that an animal wants, but does not need) nor does it result in a positive welfare balance. Short- and long-term assessments are required to identify these environmental enrichments, such that use of the item (i.e. pleasure) must be sustained. We acknowledge that such environmental enrichments provide positive hedonistic experiences (i.e. reward and pleasure) which may be independent to experiences of negative affect (i.e. fearfulness, anxiety). Therefore, it is important to note that environmental enrichments in this category do not impact survival or biological functioning, rather they exceed basic needs and may be termed ‘luxury’ items (Fraser & Duncan Reference Fraser and Duncan1998). The positive experiences provided by this environmental enrichment are not adequate to outweigh the negative experiences (i.e. hence there is evidence of positive hedonic experiences but no evidence of long-term positive welfare balance such as increased stress resilience or positive mood). This category may be particularly important as baseline environments evolve (i.e. as resources for basic needs are considered ‘housing’ rather than ‘enrichments’). The importance of this category may also be apparent for environments that have limited options to provide enrichment to meet basic needs (i.e. space). As such, with this category of environmental enrichment we acknowledge that not all of an animal’s needs must be met for it to experience pleasure but experiencing pleasure is an important component of animal welfare, even if the positive experiences are not enough to result in an overall positive welfare balance.

Some environmental enrichments that enrich for pleasure can be associated with risks to physical health. This may seem counter-intuitive but, if the risk can be managed, the environmental enrichment can still benefit animal welfare. The provision of access to an outdoor range for chickens provides a good demonstration of this point. Some individuals are highly motivated to frequently access the outdoor range (Larsen et al. Reference Larsen, Cronin, Gebhardt-Henrich, Smith, Hemsworth and Rault2017), suggesting one or more components of the outdoor area is something that they want. However, there may also be negative consequences of range access such as the presence of predators and risks of disease (Campbell et al. Reference Campbell, Bari and Rault2020). Enrichments that provide animals with something that they want, but may cause additional stress or injury (e.g. through increased aggression) also fall into the category of environmental enrichment for pleasure with risk. For example, sows are highly motivated to utilise straw but providing straw in a rack (i.e. as a point source material) results in competition to access the enrichment with dominant sows delivering increased aggression to monopolise the resource (Elmore et al. Reference Elmore, Garner, Johnson, Kirkden, Richert and Pajor2011). Environmental enrichments for pleasure that are associated with increased risk require additional management inputs (and thus additional economic inputs) to reduce the associated risks. Of note, some risks may be too great to consider regardless of other positive welfare outcomes, for example, dilution of medications due to nutritional enrichments or string causing necrosis after being caught on legs or tongues (Schlegel & Brash Reference Schlegel and Brash2015).

Enriching for pleasure does not improve biological functioning or long-term health (i.e. stress resilience) which are both associated with economic returns. Unless there is an economic return (e.g. premium price paid for free-range eggs), this enrichment may be impractical for the producer to implement and thus not effective, see section below on economics.

Environmental enrichment for a positive welfare balance

Environmental enrichment for a positive welfare balance results in long-term accumulative effects of positive experiences for animals, such as that outlined by Rault et al. (Reference Rault, Hintze, Camerlink and Yee2020) in their Vienna framework, suggesting that animals provided with this type of environmental enrichment have a positive welfare balance (i.e. positive experiences outweigh the negative experiences throughout their life). Environmental enrichments in this category provide hedonistic positive experiences to animals which are short-term experiences, but the accumulative effects of such positive experiences and/or a reduction in negative affective experiences result in improved stress resilience, increased flexibility and adaptability to stressors or positive moods. Of note, such outcomes may be achieved not just via accumulative experiences of pleasure, but also include the positive effects of agency and improved cognition associated with the provision of some environmental enrichments.

Animal welfare assessments

Prior experience with an enrichment can impact the response to enrichment later in life. For example, piglets reared in barren environments and weaned into enriched environments show evidence of improved welfare. However, piglets reared in enriched environments that are weaned into barren environments have compromised welfare (i.e. less play and more belly-nosing), even in comparison to piglets both reared and weaned in barren environments (Oostindjer et al. Reference Oostindjer, van den Brand, Kemp and Bolhuis2011). Similarly, hen welfare can be compromised if adult production environments contain specific enrichments (i.e. perches) that are not available in the rearing environment (Hester et al. Reference Hester, Enneking, Haley, Cheng, Einstein and Rubin2013). As such, the impact of environmental enrichment items and programmes must be assessed at multiple times in an animal’s production life. For our framework this includes short- and long-term assessments. Of note, the timing of such assessments will be species-specific; i.e. meat chickens lifespan is typically 4 to 6 weeks of age whereas feedlot cattle and laying hens typically live for over 1 to 1.5 years and may be kept in various housing (i.e. pasture to feedlot or rearing sheds to free-range sheds). Long-term welfare assessments measure positive welfare balance (i.e. stress resilience, mood) and pleasure associated with utilisation of the enrichment (ensuring no habitation occurs) and short-term assessments measure biological functioning (reproduction, growth, morbidity and mortality) which may be specific to one part of an animal’s life (i.e. rearing environments or parturition).

Economics

Once an enrichment has been shown to have positive outcomes for animal welfare, it must also be considered economical. In our survey, cost was ranked as the most influential barrier for enrichment implementation by industry stakeholders (Figure 1) despite the positive perception of enrichment for animal health and farm profitability (Figure 2). This relates to the nature of the welfare outcomes and cost of enrichment implementation (e.g. costs of material and labour). The cost of enrichment implementation will depend not only on the enrichment itself but also on the size of the enterprise, geographical location, and housing system and therefore will need to be calculated and considered for each application. We propose that the return on investment is reflected by the welfare outcome (discussed below) and should be considered when developing or revising minimum requirements for welfare policy and third-party quality assurance schemes.

Although production is not always associated with improvements to animal welfare, and vice versa, it is widely accepted that the physiological stress response can impact product quality and/or quantity (see Roberts Reference Roberts2004; Hemsworth & Coleman Reference Hemsworth and Coleman2011). We propose that enrichments that lead to improvements to the basic needs of an animal and enrichments that provide a positive welfare balance, will be more likely to have a positive economic return due to improvements to productivity. For example, enrichments that improve biological functioning and/or health will impact fitness traits that are associated with increased productivity (i.e. reproduction and growth) and environmental enrichments resulting in an overall positive welfare balance (i.e. stress resilience and adaptation) are expected to reduce the effects of stressors (i.e. psychological or disease) diverting energy towards productivity and/or reducing morbidity and mortality. However, to be profitable, the improvement to biological functioning (and productivity) must be sufficient to offset the cost of implementation (e.g. materials, labour for placement and maintenance and disposal).

While there is always a chance that enrichments providing pleasure may show associated improvements to productivity, it remains an unlikely outcome. As such, the cost of implementation may outweigh the benefits unless the improvements to welfare are subsidised for the producer — particularly if the environmental enrichments are associated with risks to physical health that require additional management inputs/costs. A third party accreditation scheme (e.g. conformity audit according to an animal welfare standard and provision of certification labels) may also be needed to ensure that consumers receive the required signals (e.g. trusted labels) indicating that enrichments that improved animal welfare were implemented in the livestock production process. This is a further cost to livestock producers. Consumers may be required to pay a price premium for the livestock product they demand for this approach (e.g. enrichment implementation and standard conformity accreditation) to be commercially viable for livestock producers. Further investigation into the public perception of environmental enrichments for meeting basic needs, pleasure and positive welfare balance (however the improvements are phrased to the public) and the willingness to pay for such products is required to ensure that science-based improvements to animal welfare through the provision of enrichment is economically feasible for producers to implement.

An economic benefit-cost assessment of animal enrichment implementation should also consider the broader benefits for producers. For example, by implementing enrichments, businesses will likely gain access to a broader range of retailers in higher market segments which increasingly set private standards for animal health and welfare in the production process (Fraser Reference Fraser2006; More et al. Reference More, Hanlon, Marchewka and Boyle2017). The adoption of effective enrichments can also contribute to gaining/maintaining agri-businesses’ social licence to operate (Martin & Williams Reference Martin and Williams2011). Lastly, livestock businesses may be rewarded for their implementation of enrichments through easier access to finance, since financial institutions are increasingly basing their investment decisions on sustainable production processes (Akomea-Frimpong et al. Reference Akomea-Frimpong, Adeabah, Ofosu and Tenakwah2021) such as improved animal welfare for production animals.

Practicality

We proposed that if an environmental enrichment is impractical to source, maintain or dispose it will never be implemented regardless of the impact on animal welfare. This includes providing an enrichment in a way that it can be effective, for example, ensuring enrichments are accessible to all animals (i.e. enrichment density) and/or provided at the appropriate time/age and frequency. The industry survey identified four main parameters regarding practicality that must be considered for the environmental enrichment to be effective (Table 3). These included how the direct or indirect waste from environmental enrichments could be removed, biosecurity risks, unmanageable interruptions to critical standard practices and the ability to source the environmental enrichment in the quantity and location required. Perceived issues of practicality must be addressed and considered by researchers and regulatory bodies when designing, investigating or prescribing enrichment programmes. Issues with practicality may be overcome with additional research and development (R&D), advances in technology or simply by providing scientific-based evidence to eliminate perceived impracticalities.

Table 3. Four main themes reflecting the practicality of environmental enrichment provision in Australian intensive livestock industries and industry-specific quotations

Case studies from the scientific literature

We apply the results from common environmental enrichment items reported in the scientific literature for meat chickens, gestating sows, feedlot beef cattle and laying hens, (sand, straw, brushes and perches, respectively) as an example of how our proposed framework may be utilised to communicate the benefits of each environmental enrichment to livestock welfare (see Table S4).

The scientific literature suggests, based on the available evidence, that sand is a form of ‘pseudo-enrichment’ for meat chickens. Meat chickens prefer sand over other substrates, but the use of sand is not sustained nor is there any evidence of improved biological function or positive welfare balance, unless it is paired with a suite of other enrichment items. When sand is provided with PECKStone^TM (Vilofloss, Federicia, Denmark), perches and novel objects there is evidence that meat chickens’ mood (and therefore positive welfare balance) is improved (Table S4). This enrichment programme would therefore be considered ‘environmental enrichment for a positive welfare balance.’

Literature reporting the effects of nesting materials provided to pregnant sows around the time of parturition show that hessian sacks (although used short-term) are a form of ‘pseudo-enrichment’ with no improvements to biological functioning. Conversely, straw (depending on how and when it is offered) generally improves biological functioning, evidenced by a reduction in glucocorticoid concentrations and improved reproduction (Table S4). With nesting enrichments only provided around parturition, it is unlikely that these effects will result in long-term positive welfare balance of the sow’s life, however this remains unknown. Based on the current available literature, the provision of straw to sows close to partition would be classified as an ‘enrichment for meeting basic needs.’

The scientific literature suggests that perches (in isolation) enrich laying hen environments for pleasure. Hens are motivated to access perches and their use is sustained until the end of the production cycle, but there is no evidence that they improve biological functioning or long-term positive welfare balance (Table S4).

There is a lack of investigations that utilise both short- and long-term assessments of suffering, pleasure and welfare balance after the provision of environmental enrichment (Table S4). We propose that future investigations of environmental enrichment study suffering, pleasure and welfare balance throughout the animal’s lifecycle, as outlined in Table 2. Applying the framework to the current literature, the true impact of environmental enrichments on animal welfare may be underestimated, as it is clear from Table S4, that long-term assessments of positive welfare balance (i.e. stress resilience and positive mood) are under-researched and under-reported.