Animal welfare science: an integral piece of sustainable insect agriculture

The insects as food and feed (IAFF) industry represents one of the largest undertakings of industrial livestock rearing in human history, with at least a trillion animals reared each year and massive growth potential. As other livestock industries have grown, animal welfare science has become an essential field for maintaining socially responsible, ethical, and sustainable industry practice. Like traditional livestock industries, the IAFF industry could also benefit – ethically, socially, and economically – from a field of welfare science. Here, we present three economic reasons for considering animal welfare in intensive production systems: (1) improving production outcomes, (2) maintaining social license to operate, and (3) differentiating products. In each case, we provide examples from established livestock industries that highlight how the field of animal welfare science can benefit producers. Further, we provide examples of how the IAFF industry would benefit from the support of a dedicated field of welfare science. We end by calling attention to key partnerships between entomologists, welfare scientists, and producers that could advance the common goals of these stakeholder groups, as well as animal welfare in insect agriculture.


Introduction
The insects as food and feed industry (IAFF) aims to help sustainably solve the growing protein crisis, where 10.9 billion people must be fed by 2100 (United Nations, 2013;van Huis and Tomerlin, 2017).The industry already rears at least 1 trillion insects a year (Rowe, 2020), making it possibly the largest undertaking of mass-reared animal agriculture in human history.For comparison, about 79 billion birds and land mammals are slaughtered for meat each year (FAOSTAT in Šimčikas, 2020).The industry is in its early days, with significant potential to grow: for instance, replacing 25% of fishmeal with insect protein results in roughly 40-80 trillion insects slaughtered each year (Rowe, 2020).Eventual 'worldscale' facilities are expected to produce more than 1 million tons of insect protein each, or about 15 trillion insects annually (Kok, 2017).
Many producers, consumers, and academics have expressed an interest in considering the welfare of insects as mini-livestock (Barrett et al., 2022a(Barrett et al., , 2023;;Bear, 2019;Boppré and Vane-Wright, 2019;de Goede et al., 2013;Delvendahl et al., 2022;IPIFF, 2019;Kortsmit et al., 2022;van Huis, 2021).To date, most arguments put forth for considering insect welfare are ethical ones, based on the emerging evidence that at least some insect species may be sentient and that the precautionary principle should be adopted in cases of uncertainty (e.g.Gibbons et al., 2022a;van Huis, 2021).This principle suggests that the IAFF industry treat insects as though they are sentient to avoid causing potentially significant harm to a very large number of individuals (with stronger and weaker versions of what this entails; Birch, 2017;Knutsson and Munthe, 2017).In practice, this would mean that some empirically-informed and economically-viable considerations of insect welfare should become standard IAFF industry practice.However, businesses must consider the costs and benefits associated with changing their practices (Fernandes et al., 2021), and ethical arguments alone are unlikely to drive sustainable improvements in animal welfare (Dawkins, 2017).Thus, industry adoption of these standards will depend on demonstrating the financial, not just moral, value of animal welfare.
In this paper, we describe how improvements in animal welfare can add financial value to insect production systems by: (1) improving production outcomes, (2) maintaining the industry's social license to operate, and (3) differentiating products to achieve a competitive advantage.We discuss examples from established livestock industries that highlight how the field of animal welfare science has been instrumental in supporting vertebrate livestock producers as their industries have evolved.In each case, we provide examples of how the IAFF industry could similarly benefit from a dedicated field of insect welfare science.Our intention is to reinforce, rather than replace, ethical arguments for welfare consideration, which have been described in detail elsewhere (most recently, Klobučar and Fisher, 2023;Voulgari-Kokota et al., 2023).

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What is animal welfare and welfare science?
Conceptions of animal welfare typically emphasize the animal's ability to feel well (hedonist approach), function well (functional approach), or perform natural behaviors (naturalistic approach) (Fraser et al., 1997;Weary and Robbins, 2019).While it is unclear how each of these conceptions should be weighed in welfare assessments, academics largely agree that an animal's emotions are critical determinants of their welfare and that welfare ranges along a continuum of negative to positive (Fernandes et al., 2021).Welfare is reduced by negative affective states such as pain, fear, and frustration, and increased by positive states such as pleasure (Duncan, 2008).Physical health is also important, as pathological states often produce negative affective states and impair an animal's ability to function well.However, a healthy animal may still experience poor welfare if they cannot perform positively reinforcing behaviors (e.g.interacting with other animals, or species-specific behaviors like nesting in hens; Dawkins, 1988;Hemsworth and Edwards, 2021).Put simply, an animal experiencing good welfare is healthy and has what it wants (Dawkins, 2008).Improving animal welfare requires evaluating whether changes in animal use practices do, in fact, benefit the animal.Animal welfare science provides a systematic, evidence-based approach for assessing welfare that uses environmental, physiological, and behavioral indicators to infer an animal's subjective experience and develop strategies to improve welfare in practice, thereby informing public and private regulations.To date, animal welfare science has focused on vertebrates, particularly mammals, birds, and fish, and to a lesser degree on some invertebrates, namely cephalopods and crustaceans (Albalat et al., 2022;Pedrazzani et al., 2023;Ponte et al., 2023;Wuertz et al., 2023).However, the question of insect welfare is gaining attention in light of the emerging research on insect neuroscience and behavior, and the increasingly widespread and global practice of farming insect livestock.Thus, it is timely to consider how animal welfare science may benefit the IAFF industry.

Improving production outcomes
Although animal welfare improvements may sometimes cost money (e.g.infrastructure changes, staff training, ongoing operational costs), they can bring positive returns on investment over time through reductions in mortality and involuntary culling, improved disease resistance, and reduced veterinary/health care and antibiotic use (Dawkins, 2017;Albernaz-Gonçalves et al., 2022).Indeed, empirical studies in the dairy and pig industries have found that better animal welfare is positively, albeit weakly, associated with greater farm profitability (Henningsen et al., 2018;Villettaz Robichaud et al., 2019).Additionally, improvements in productivity simultaneously mitigate impacts to the environment and public health through reduced wastage of feed and energy (e.g.Capper and Cady, 2020).
Poor welfare conditions cause prolonged stress that can suppress the immune system and deteriorate health, in turn reducing productivity (De Passillé and Rushen, 2005).Efforts by animal welfare scientists to identify and minimize stressful management practices (e.g.overcrowding, extreme temperatures, social disruption, mal-nutrition, transport) can simultaneously promote welfare and productivity.For example, chickens and pigs that received positive handling had better productive and reproductive outcomes compared to animals that received aversive human contact (reviewed in Zulkifli, 2013).In addition, including health and welfare traits in breeding programs has been shown to be more profitable than focusing on productivity alone (Lawrence et al., 2004).For example, the dairy industry has broadened their breeding program to include welfare traits after decades of intensive selection for milk yield led to increased lameness, mastitis resistance, and lower fertility (Oltenacu and Broom, 2010;Egger-Danner et al., 2015).Economic benefits from promoting higher welfare may be even greater for insects, as some have speculated that insects will not tolerate inhumane conditions as well as vertebrates (though empirical evidence for this claim is needed; Boppré and Vane-Wright, 2019).
Welfare improvements can also benefit product quality (Dawkins, 2017).For example, providing pigs with straw and extra space resulted in higher-quality pork compared to rearing pigs in intensive housing with bare slatted floors and the minimum recommended space allowance (Beattie et al., 2000;Klont et al., 2001).Additionally, more humane handling, transport, and slaughter methods can improve meat quality by reducing bruising, injuries, and stress-induced changes in blood constituents that lead to undesirable meat traits such as pale soft meat in pigs and dark cuttings in cattle (Harley et al., 2012;Schwartzkopf-Genswein et al., 2012;Kumar et al., 2023).
While improvements in welfare can benefit productivity, this is only true up to a point, and it is a common fallacy that high-producing animals have high welfare (McInerney, 2004).Indeed, the productivity gains of modern agriculture have often come at a cost to animal welfare (e.g.confinement housing, rapid weight gain, mutilations).Practices that focus solely on productivity are likely unsustainable in the long term due to cumulative impairments to animal health and welfare (Fernandes et al., 2021), and the elevated risk of zoonotic outbreaks that carry significant economic costs (Rahman et al., 2020).Intensification of animal agriculture is a key driver of zoonotic diseases and antimicrobialresistant pathogens (Pinillos et al., 2016), principally through close confinement of many animals, genetic homogenization, stress-induced immunosuppression, and antibiotic use (Hayek, 2022).For example, higher animal welfare standards on farms and during transport reduce Campylobacter and Salmonella contamination of poultry meat, resulting in improved food safety (Ian-netti et al., 2020).Thus, a stronger focus on welfare, and not just productivity, can ultimately increase both farm profitability and product safety, as well as global sustainability by reducing feed and energy waste and mitigating disease emergence/spread among other domestic animal populations, wildlife, and humans (i.e. the One Health approach; Nabarro and Wannous, 2014).All three of these values -economic productivity, product safety, and global sustainability -are stated as cornerstones of for the IAFF industry (e.g.Tomberlin et al., 2022).
Already, the emerging literature on farmed insect welfare has contributed several promising research directions that may yield increases for economic productivity in the IAFF industry.For example, the common industry practice of not feeding breeding black soldier flies (BSF; Hermetia illucens, Diptera: Stratiomyidae) has been highlighted as a welfare concern (malnutrition and hunger; Barrett et al., 2022a;Kortsmit et al., 2022).Adults are morphologically equipped to eat, have food preferences, and live longer and lay more eggs when provided with food and water (Bertinetti et al., 2019;Bruno et al., 2019;Fisher and Romano, 2020;Klüber et al., 2023;Macavei et al., 2020;Nakamura et al., 2016;Oonincx et al., 2016).Further, feeding allows more females to lay a second clutch (Klüber et al., 2023); this increase in genetic mixing may help prevent colony collapse due to the loss of genetic diversity in rapidly-breeding managed populations (Rhode et al., 2022).In this example, welfare science changed the perspective taken on feeding practices, generating a novel insight that could improve economic productivity, following further research, through increased fecundity and reduced genetic homogenization.Alongside further information that is needed on the appropriate diets for maximizing reproduction of adult BSF, research must still account for the costs of feed or labor associated to determine any economic productivity gains for the IAFF industry.
As another example, cannibalism has been identified as both a cause and potentially a consequence of negative welfare states in farmed yellow mealworms (Tenebrio molitor, Coleoptera: Tenebrionidae), which can also impact economic productivity (Barrett et al., 2023).There is significant uncertainty about what causes high rates of cannibalism in mealworms, but it is plausible this behavior is a response to an array of welfare challenges, as has been posited for other farmed larval insects (Kortsmit et al., 2022).Inadequate hydration, malnutrition, and too-high stocking densities may all induce negative welfare states, resulting in increases in cannibalistic behavior (Hardouin and Mahoux, 2003;Weaver and McFarlane, 1990;Yang et al., 2021).Studies that assess the impacts of these variables on cannibalistic behavior may serve to improve economic productivity by increasing total insect protein yield -while reducing both the negative welfare states that induce cannibalism and the welfare issues caused by cannibalism itself (injury, disease, and mortality; Weaver and McFarlane, 1990).Solving the welfare challenges that lead to cannibalism may also avoid accidental selection in favor of cannibalistic behavior, which has occurred in other mass-reared insect larvae in laboratory conditions (Vijendravarma et al., 2013), reducing the risk of evolving increasingly economically unviable strains of mealworms.Additionally, welfare researchers may determine that techniques of selective breeding could be used to reduce cannibalistic behavior in any insect population, even if such accidental selection has already occurred.
Considering insect welfare can also help the industry anticipate and mitigate disease outbreaks (see discussions of viral, fungal, and bacterial pathogens, as well as parasitoids and parasites that affect farmed insects in Barrett et al., 2022Barrett et al., , 2023;;Eilenberg et al., 2015Eilenberg et al., , 2018;;Joosten et al., 2020;Slowik et al., 2023).For example, Barrett et al. (2022) proposed diseases as an emerging area of welfare concern for black soldier fly larvae, despite few reported incidents of disease for these animals in the scientific literature and claims that their highly adapted immune system as filth-feeding flies could prevent outbreaks.Only a few months later, a mass-mortality event of 'soft rot' -a new disease impacting industrially farmed black soldier fly larvae -was reported (She et al., 2023).It is likely that the same risk factors for disease in traditional livestock industries apply to the IAFF industry.In addition, even if insects pose lower risks of zoonotic diseases than vertebrate livestock, we don't know how those risks may change as farming scales.Including welfare in species-specific management decisions, rather than merely focusing on productivity, will be important in preventing disease and raising resilient animals.
These aforementioned cases are just a few of many examples from the emerging field of insect welfare that demonstrate how the novel perspective welfare science takes on insect livestock rearing could also improve economic productivity, as in traditional livestock industries.However, while many improvements in animal welfare may align with better production outcomes, others may have no benefit or even conflict with production goals (Ritter et al., 2019).Rather than deprioritizing welfare in these situations, it is worth considering the broader and more indirect economic benefits that extend beyond production gains, as we discuss in the next sections.

Maintaining social license to operate
Animal welfare has become critical for animal-use industries to maintain their social licenses to operate, which refers to the implicit approval a community gives an industry to conduct its current business practices.As public concern for animal welfare grows, traditional animal agriculture has been targeted by undercover investigations and advocacy campaigns from animal protection groups (e.g.O'Kane, 2019).These efforts have led to regulatory bans of contentious practices, such as cage confinement of egg-laying hens, sows, and veal calves in many western nations (Shields et al., 2017).In addition to increased regulation, litigation, and consumer demands, erosion of public trust threatens sales volumes and, in some cases, can lead to market collapse, as occurred with the live cattle export industry in Australia (Windsor, 2021).Some animal agriculture industries have approached these concerns as a public relations issue; they recognize that a threat to their social license exists but attempt to deflect concerns through public relations campaigns (Hampton et al., 2020).A common idea is that the public needs more and better information and their concerns can be fixed through one-way education efforts (Weary and von Keyserlingk, 2017).However, research indicates that learning about livestock practices fails to improve acceptance for many people (shown specifically for insects as livestock feed in America: Fukuda et al., 2023), and in some cases may increase criticisms (Ryan et al., 2015;Ventura et al., 2016).Secrecy is also not a solution -the public expects transparency about how animals are treated and industry efforts to silence whistleblowers (so-called ag-gag laws) erode public trust (Robbins et al., 2016).
An established approach to mitigate risk is to engage in transparent, two-way dialogue with the public (Weary and von Keyserlingk, 2017).This type of communication can build public trust and allow industry stakeholders to identify common ground and areas for compromise.Industries can also mitigate threats to their social license by proactively engaging with animal welfare scientists to identify practices of welfare concern and implement practical solutions.As crises can unfold rapidly, anticipating concerns can help to avoid rash political interventions that are not always in the best interest for the animals and can cause considerable upheaval for producers (e.g.Savory, 2004).For example, the U.S. dairy cattle industry has taken proactive, science-informed measures to bring their practices better in line with public expectations, such as banning tail-docking and mandating pain relief for disbudding/dehorning (National Milk Producers Federation, 2020).By acting proactively and engaging with welfare scientists, the industry may maintain societal support and thus more control over changes that occur.
Animal welfare scientists also have a key role to play in building consensus and trust between industry and public.Animal welfare science can help manage divergent perceptions between stakeholders about what they think animals need vs what matters to the animal.For example, naturalness is a prominent value held by the public, however natural living does not ensure that farm animal welfare is improved (Dawkins, 2023).Natural environments can promote behaviors associated with good welfare, such as grazing, but can also expose animals to adverse conditions, such as heat stress, predation, or malnutrition.Welfare science helps to determine what aspects of natural living matter to the animal and can inform public and industry discourse on this topic.This role of welfare science in helping producers manage divergent perceptions is likely to be especially important for animals that are more evolutionarily distant from humans (e.g.insects), as their welfare needs are unintuitive and thus especially likely to be misunderstood by an unfamiliar public.For welfare standards to be sustainable, a compromise must be reached among the values of all stakeholders, namely the animals, producers, and the public (Weary et al., 2016).
There is currently very little literature on how the public perceives animal welfare in the growing IAFF industry (reviewed in Delvendahl et al., 2022, and see Fukuda et al., 2023, Dullaghan et al., 2021).Broadly, these studies suggest that concern for insect welfare is not negligible, despite some confusion, and that concern for insect welfare may grow over time.Demonstrating confusion amongst consumers, Polish adults were most likely to answer 'I don't know' when asked if entomophagy would help overcome animal welfare issuesfollowed by a close split between 'yes' and 'no' (Orkusz et al., 2020).Similarly, vegetarians and omnivores both viewed entomophagy as more ethical than eating conventional livestock, suggesting less concern for the welfare of insects when used as food than for other farmed animals.However, this trend did not extend to vegans (Elorinne et al., 2019).
Further, more recent results from the USA on the use of insects as livestock feed suggest consumer atti-tudes on the likelihood of insect sentience may be shifting.A survey of ~4,500 U.S. adults found 52-65% believe insects can feel pain, depending on the focal species (Dullaghan et al., 2021); another, smaller survey of American adults found 47.2% of the general population believed insects could feel pain (species unspecified; Fukuda et al., 2023).Additionally, 58% of American adult consumers opposed to the use of insects as livestock feed cited ethical concerns, and, of those opposed, 73.6% believed insects could feel pain.Consumers with concerns about pain were more likely to be young, representing the future consumers of IAFF industry goods, and self-reported that they were knowledgeable about industry practices (Fukuda et al., 2023).This suggests that greater awareness of the industry would not address consumers' ethical opposition; instead, implementing high welfare practices may be necessary to shape public perception.Altogether, these data suggest that the group of consumers most important for shaping social acceptance and legislation of the IAFF industry in the future are among those most concerned with the industry's welfare practices.Further research is also needed to better understand if public concern of insect welfare in the IAFF industry differs based on species or life stage as, for example, data suggests the public are less confident termites can feel pain than bees or ants (Dullaghan et al., 2021); no studies have yet assessed the major insect species farmed as food and feed.
In addition to establishing expectations for insect rearing practices, it is possible that public perception will also shape guidelines on how insects are fed to livestock.Providing live larvae as feed can benefit poultry and pig welfare, allowing the expression of natural foraging behavior, reducing aggression, and improving health (Ipema et al., 2020;Ipema et al., 2021).However, this practice likely has significant welfare repercussions for the insects, including stress due to transportation, introduction to novel environments, injury, and predation.It is unclear how to scientifically compare subjective experiences between species, or how the public will trade off the perceived costs and benefits of feeding live larvae to livestock on animal welfare.A survey of Italian meat consumers found that the main factors in their decisions to purchase insect-fed poultry were the same regardless of whether insect meal or live insects were provided (Sogari et al., 2022).However, consumers overwhelmingly care about end-of-life practices in other livestock industries (Sinclair et al., 2023), and transport and slaughter are the most strictly regulated practices in animal agriculture (Caporale et al., 2005;Mench, 2008).Thus, the IAFF industry may benefit from proac-tive research and engagement in slaughter reform, with implications for how insects are fed to livestock, to continue to meet evolving consumer expectations.
UK insect producers also believe consumers care, or will care, about insect welfare, particularly during slaughter (Bear, 2019).Their intuition is borne out by the building attention of the popular press to slaughter (e.g.Carlson, 2023;Reynolds, 2023;Sebo and Shukraft, 2021), as well as increased focus by animal advocacy groups (e.g.EuroGroup for Animals, 2023).There has even been greater attention paid to invertebrate welfare, and the evidence for insect sentience, by policymakers, due to the growing trend of farming invertebrates (e.g.Council of Animal Affairs, 2018;DEFRA, 2023;Birch et al., 2021 and impacts on the UK Animal Welfare (Sentience) Act 2022).
Alongside public sympathy for, and legislative discourse around, insect welfare in many European and North American countries, there appears to be increasingly sound evidence for insect sentience, suggesting it is unlikely the industry will see a massive reversal in public judgments about insect welfare in response to new scientific information.Admittedly, empirically assessing sentience in any nonhuman animal is challenging, but it is particularly difficult for animals that are phylogenetically, physiologically, anatomically, and behaviorally distant from humans, like invertebrates (Birch, 2020).Nevertheless, it is generally agreed upon that accumulating neurobiological and behavioral evidence can help distinguish the experience of negative subjective states, such as pain, from reflexive responses, like nociception, that can occur without pain (Birch et al., 2021;Crump and Birch, 2022;Smith and Boyd, 1991).
Insects of several orders meet many of the criteria relevant to sentience (criteria developed in Crump et al., 2022, adapted from Smith andBoyd, 1991; over 300 studies reviewed for insects in Gibbons et al., 2022a).Insects have sensory cells called nociceptors that respond to a range of noxious stimuli (Caron et al., 2020;Grueber et al., 2001;Khoung et al., 2019;Tracey et al., 2003).They possess dedicated sensory integrative brain regions (Homberg, 1987;Thiagarajan and Sachse, 2022), and nociceptive information reaches those regions (Aso et al., 2012;Emanuel and Libersat, 2019;Galili et al., 2014;Hu et al., 2018;Rana et al., 2022).Insects' behavioral responses to noxious stimuli are modulated by endogenous and exogenous chemicals that affect the nervous system in ways that are consistent with the hypothesis that negative affective states are being attenuated (Araujo et al., 2021;Hibicke and Nichols, 2022;Jang et al., 2023;Manev and Dimitrijevic, 2004; but see Groening et al., 2017, while noting that insects have no opioid receptors, Mirabeau and Joly, 2013).The most evidence for insect pain has been found in the adult Blattodea (cockroaches, termites) and Diptera (flies, mosquitoes; Gibbons et al., 2022a), which both include farmed species used as livestock or pet feed.
Some insects are capable of self-protective behaviors (Hentschel and Penzlin, 1982;Jang et al., 2023;Walters et al., 2001;but see Eisemann et al., 1984, with comments by Gibbons andSarlak, 2020) and motivational tradeoffs in response to harmful and rewarding stimuli (Gibbons et al., 2022b;Kaun et al., 2011;Manev and Dimitrijevic, 2004).Many can learn in association with noxious stimuli, including more complex forms of learning like trace conditioning and reversal learning (Grover et al., 2022;Longo, 1964;McCurdy et al., 2021).Some research directly suggests insects may possess affective states (Bateson et al., 2011;Solvi et al., 2016).Finally, some insects can perform surprisingly sophisticated behaviors including social learning, individual recognition, forming abstract concepts of 'same' and 'different' , numerical cognition enabling addition and subtraction, and tool use (Alem et al., 2016;Howard et al., 2019;Pierce, 1986;Sheehan and Tibbetts, 2011;Weise et al., 2022).Notably, cognitive abilities are separate from sentience -intelligence is not a prerequisite for an ability to feel -however advanced cognition may still prove relevant to the public's perception of insect pain and sentience.While none of the aforementioned evidence proves insect sentience, it makes it plausible, particularly at the adult life stage where significantly more research has been conducted (see Gibbons et al., 2022).Notably, significant differences in nervous system organization and behaviors between the adult and juvenile life stages (e.g.Barrett et al., 2022b for black soldier flies) means that research on sentience (and public perceptions) should be conducted throughout development.More data on consumer perceptions of welfare in relation to specific species and life stages, IAFF messaging strategies, feed vs. food contexts, and consumer populations with different demographics, is clearly necessary.However, the research to date suggests there is a role for animal welfare science in managing public perceptions of, and thus potential opposition to, the IAFF industry.How industries respond to public concerns can shape the market opportunities and long-term survival of affected industries.Strategies emphasizing proactivity and transparency through collaborations with welfare scientists appear to have been successful in repairing and protecting social licenses in other industries (Hampton et al., Journal of Insects as Food and Feed 0 (2023) 1-15 Downloaded from Brill.com 12/20/2023 07:15:06AM via Open Access.This is an open access article distributed under the terms of the CC BY 4.0 license.https://creativecommons.org/licenses/by/4.0/2020) and are likely to be critical for risk mitigation in the IAFF industry as well.

Differentiating products
While animal welfare is an important source of risk for animal industries (e.g.media scandals, public scrutiny), it also presents an opportunity for product differentiation and long-term value creation.Citizens increasingly care about animal welfare, and studies have shown that consumers are willing to pay a modest premium for products with higher animal welfare attributes, such as increased space per animal and pasture access (Bir et al., 2020;Clark et al., 2017).At the same time, consumers face a number of challenges when shopping that can lead to a discrepancy between attitudes and reallife purchasing behavior, including difficulty processing information on products, having to choose among different product attributes (e.g.taste, nutritional value), and balancing values with affordability and availability (Cornish et al., 2019;Hyland et al., 2022).Nevertheless, there is a growing market for higher welfare foods, as evidenced by increased sales of animal products with welfare claims in recent years (Amos and Sullivan, 2018).
In addition, many of the world's largest food companies, like Nestlé, McDonald's, and Unilever, have published formal policies outlining their commitment to purchasing from suppliers with higher-welfare products (Amos et al., 2022).Their program standards may follow company-specific schemes (e.g.Danone's Dairy Animal Welfare Program) or third-party certification programs such as RSPCA Assured, Global Animal Partnership, or Certified Humane.
Importantly, differentiating products based on welfare attributes can be a source of risk for companies if their claims are fraudulent or misleading.Multiple companies and industry associations that have used phrases like "humanely raised" and "happy cows" on packaging and in advertisements have been challenged in lawsuits filed by animal and consumer advocacy groups (Carman, 2022;Jacobs, 2021).Although in many cases these lawsuits are dismissed, the media exposure can damage the company's reputation and draw increasing scrutiny of all animal welfare claims (Spain et al., 2018).Thirdparty audits can help strengthen a company's assurances by providing an objective certification of their veracity and are trusted more by the public than firstor second-party assessments (Spain et al., 2018).Regardless of who performs the audit, the program's standards must be based on empirical and measurable evidence to ensure genuine improvements for the animals.
In the IAFF industry, it is unlikely that markets for higher animal welfare will emerge quickly, if at all, particularly for products that are not marketed for direct human purchasing (e.g.livestock feed).However, there may be opportunities for product differentiation where products are destined for human consumption (e.g.cricket flour) or for incorporation into pet food (a consumer base that may be more interested in animal welfare than the average member of the public).The most useful approach may be to integrate animal welfare into broader quality assurance programs that may appeal to consumers who have a modest interest in animal welfare but would not pay a premium for it as an individual food attribute (Heerwagen et al., 2015).Early adoption of science-based, third-party-validated insect welfare standards could also give companies a first-mover advantage by positioning them to develop exclusive agreements with customers that value animal welfare ahead of their competitors.In addition, with the rise of socially responsible investment and the recognition of poor animal welfare as a business risk, companies with high animal welfare standards may have a competitive advantage with some investors (Amos and Sullivan, 2018).

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Growing a field of insect welfare science Independent of ethical considerations, improved animal welfare can increase productivity, mitigate risk by building and maintaining public trust, and provide opportunities for product differentiation and competitive advantage.We recommend five key approaches for moving the IAFF industry forward in growing an empirical field dedicated to developing and reinforcing practices that promote animal welfare and industry sustainability: 1.
Collaboration:  (Barrett and Fischer, 2023).Week-long intensive courses and smaller workshops, run by teams of industry producers and independent academics, could build the field to meet industry needs.Longer-term collaborations could involve internships and training programs with dedicated insect welfare programs at universities.2. Funding research: Some questions in the field of insect welfare are particularly likely to be economically viable for producers.Funding independent scientists to conduct these studies can grow the field, demonstrate commitment to animal welfare, and encourage transparency.For example, dairy organizations in North America (e.g.National Milk Producers Federation, Dairy Farmers of Canada) offer grant and graduate student scholarship programs to support research topics of interest to the industry, including animal welfare.Producers may not have to do all this funding themselves; they may also advocate for greater governmental research funding to be spent on the IAFF industry broadly, and insect welfare specifically (Tomberlin et al., 2022).For instance, the USDA NIFA Agriculture and Food Research Initiative funds research on agricultural animal welfare -but only vertebrate-focused proposals are currently considered due to legislative barriers (Barrett, pers.comm.).Producers and insect welfare scientists are aligned as stakeholders in demonstrating that government spending on insect welfare research could be beneficial for our agricultural systems, environment, economy, human health, and for the animals themselves.3. Management: Many major food companies report senior management oversight and employee training on animal welfare (Amos et al., 2022).In-house welfare scientists can contribute to research and development and identify emerging welfare concerns and solutions.They can also provide animal welfare training through onboarding and ongoing employee education programs, and develop and communicate standards of animal care to the public and stakeholders.4. Self-Regulation: Several trade associations representing livestock producers have developed voluntary animal welfare standards in consultation with independent animal welfare scientists.For example, more than 99% of the U.S. milk supply comes from farms participating in the National Milk Producers' Federation FARM program.This program sets standards for animal care, including space requirements, pain relief for painful procedures (e.g.disbudding), and benchmarks for diseases and injuries (National Milk Producers Federation, 2020).These policies can be routinely updated with input from animal welfare scientists and industry stakeholders to demonstrate the industry's commitment to science-based best practices (e.g.every three years for FARM).Although it will take time to develop accreditation systems, integrity of the program could eventually be ensured through regular on-site third-party audits and public performance reports -strengthening public trust in the long-term.5. Transparent communication: Transparency is key to earning and maintaining public trust and generating sustainable empirical solutions to welfare challenges.The IAFF industry will benefit from proactively communicating with retailers, consumers, investors, and animal welfare scientists about animal care and providing clear evidence of welfare improvements.Candid two-way dialogue will be needed to understand stakeholder expectations and reach a consensus on best practices for animal welfare.While secrecy to protect economically valuable innovations is often the norm in fast growing industries, a lack of transparency about animal welfare could negatively affect the entire industry's social license to operate.By proactively communicating about insect welfare, and engaging in open data sharing, the industry can help grow a community of experts while earning, and maintaining, public confidence.By engaging in these five practices, producers can assist in building the emerging field of insect welfare, an opportunity that aligns with the values of good resource stewardship and ethically conscious practices that are hallmarks of the industry's identity around the world.By taking an active role in growing the field, the IAFF industry will get timely feedback on welfare improvements as facilities scale and innovate.Critically, this gives producers the opportunity to address welfare challenges preemptively (e.g. during facility design) rather than retrofitting existing facilities, as has been the case in many livestock industries.As traditional livestock industries demonstrate, animal welfare is an integral part of a successful business strategy and deserves the same consideration as any other investment to sustain the industry.By embracing this lesson, the IAFF industry can make informed decisions to build a sustainable and socially responsible industry from the start.
Journal of Insects as Food and Feed 0 (2023) 1-15 Downloaded from Brill.com 12/20/2023 07:15:06AM via Open Access.This is an open access article distributed under the terms of the CC BY 4.0 license.https://creativecommons.org/licenses/by/4.0/ Journal of Insects as Food and Feed 0 (2023) 1-15 Downloaded from Brill.com 12/20/2023 07:15:06AM via Open Access.This is an open access article distributed under the terms of the CC BY 4.0 license.https://creativecommons.org/licenses/by/4.0/ ing out welfare research on commercial farms, as occurs in other livestock industries, can also allow the simultaneous study of other factors, such as food safety, to ensure improved animal welfare processes are sustainable in the broader context of societal values, such as human and environmental health.