Welfare of exotic pets - evidence: scoping review

Results

Evidence for compromised welfare is presented in the following order:

i) Capture or breeding

ii) Transport and handling

iii) Behaviour (behavioural needs and evidence of abnormalities in captivity)

iv) Conditions in commercial premises

v) Housing requirements

vi) Nutrition

vii) Health and disease

viii) Mortality

For some animals, no information was found for some or even most of the headings. Where information was only available on the behaviour of animals in their wild habitat, this was not included. Headings are only used where relevant evidence is available (see table of contents).

The licensing of pet breeding and trading is set out in the Scottish statutory instrument: “The Animal Welfare (Licensing of Activities Involving Animals) (Scotland) Regulations 2021”. This statute makes specific provisions for dogs, cats and rabbits (schedules 6-8), but the requirement for licensing, and the duty to provide appropriate care, record keeping and information to owners applies to all the species in this review apart from fishes.

Sections of the general guidance may be particularly difficult to apply to exotic pets, e.g., in schedule 2 “If the animals are kept in premises from which the licensable activity is carried on, active and effective environmental enrichment must be provided to the animals in inside and any outside environments” and in schedule 3: “For species whose welfare depends partly on exercise, opportunities to exercise which benefit the animals’ physical and mental health must be provided”. Where there is no objective, published evidence on what level of exercise is conducive to good welfare, nor on suitable enrichment which provides animals with control over their environment, as well as exercise and expression of normal behaviours, it is difficult to see how compliance will be achieved.

Captive-bred animals can be privately traded and imported but must meet IATA live animal regulations (LAR) (https://www.iata.org/en/publications/store/live-animals-regulations/).

No results about pets

For the following mammalian species, there was no information on the welfare of these animals as owned by private individuals in Scotland or the rest of the UK. Where literature relevant to their health and welfare was found, it relates only to animals in zoos, laboratories, or sanctuaries.

Carnivores

• Coatis
• Leopard cats
• Meerkat
• Ocelot
• Serval

Primates

• Tamarins
• Squirrel monkeys
• Marmosets
• Lemurs
• Capuchin monkeys
• Bushbabies

Marsupials

• Wallabies
• Sugar glider

Rodent

• Chipmunks

1.0. Mammals

The welfare of mammals kept as pets in the UK is affected by their origin and journey to the UK. The licensed trade in exotic pets gives an indication of which species are most commonly kept in the UK (Elwin et al., 2020). Licenses held by UK traders selling mammals most frequently listed chinchillas (301 listings; max. number = 3052) and degus (283 listings; max. number = 3056). Also for sale were hedgehogs/African pygmy hedgehogs (28 listings; max. number > 357), sugar gliders (10 listings; max. number = 89), opossums/short-tailed opossums (two listings; max. number = 65), skunks (five listings; max. number of individuals=48), genets/West African large spotted genets (two listings; max. number>2), and primates (including, e.g., marmosets and ring-tailed lemurs). Between 2014 and 2018, 75% of non-CITES wildlife imports were rodents and 19.5% were lagomorphs (Green et al., 2020). In this period, 943 individual carnivores were imported from 47 countries across seven different regions, according to the APHA database.

Another general issue affecting the welfare of exotic pet mammals is iron storage disorder, which is believed to occur because of a discrepancy between wild and captive diets. This condition is diagnosed at necropsy where transferrin saturation occurs in the liver (Clauss and Paglia, 2012). However, the clinical relevance of excess dietary iron (which may be supplemented inadvertently in combined mineral supplements) across many species is yet to be determined. Screening programmes and experimental studies of the effect of diet on health are required to determine the significance of this issue for captive mammals.

1.1. Insectivores

1.1.1. African pygmy hedgehog, Atelerix albiventris

Using the pre-defined search terms, only 30 results were found on Web of Science (WoS). Most studies described clinical illness in hedgehogs or referred to their potential to carry zoonotic disease, including fungal skin infections and antibiotic-resistant Salmonella (see appendix 1).The most cited illnesses are neoplasia (Diaz-Delgado et al., 2017; Go et al., 2019; Kondo et al., 2019; Siddle et al., 2021; Singh et al., 2006; Song et al., 2014; Wozniak-Biel et al., 2015) and skin disease (Han et al., 2011; Iacob and Iftinca, 2018; Pantchev and Hofmann, 2006; Romero Nunez et al., 2019; Romero et al., 2015).

Bament and Mancinelli (2014) published veterinary guidance on the care of pet African pygmy hedgehogs. They are nocturnal and males cannot be kept together due to aggression. Climate is a key factor, which prevents these hedgehogs from living outdoors for most of the year in Scotland (they enter a state of torpor below 18°C), but in wild conditions they will swim, climb, dig and live in burrows during the day (Johnson, 2010). Veterinarians cite obesity as a common problem (Hedley, 2011; Bament and Mancinelli, 2014), but its prevalence in the UK pet population is not known.

Neoplasia was present in 60% of pet African pygmy hedgehogs submitted for necropsy in a Japanese study (Okada et al., 2018). Raymond and Garner (2001) found similar results, in hedgehogs presented to an American pathology lab (HCS/ZooPath); 53% of the animals between 2 and 5.5 years of age had at least one tumour type, while 8.6% of the animals had more than one tumour type”. Other health concerns include the neurological abnormality, “Wobbly hedgehog syndrome” (WHS), which is associated with inbreeding and low genetic diversity (Thompson et al., 2020). WHS is progressive and associated with a poor prognosis (Hedley et al., 2013).

Owners do not always recognise symptoms of illness until they are posing severe harm to welfare. Thompson et al. (2020) described a case of WHS presented to a veterinary teaching hospital (Hokkaido) for diagnosis with a three-week history of illness, and which had progressed to tetraparesis (inability to stand or roll into a ball) and gangrene. A 3-year-old hedgehog presented at Mahidol University with advanced neoplasia “suddenly developed screaming, gasping for air and lethargy shortly before dying” and was presented for necropsy.

No other search terms yielded information about the welfare of these animals in breeding, transport, commercial premises or as pets.

Summary: African pygmy hedgehogs

Biological or behavioural needs which are difficult to provide in captivity.

• Adapted to a warm climate
• Broad behavioural repertoire (digging, climbing, swimming)
• Predisposition towards neoplasia (cancer).

Evidence of harm associated with captivity.

• Little information on the conditions in which pet African pygmy hedgehogs are bred, traded and owned.

More information is needed to understand the welfare of this animal.

• Males, kept in isolation to avoid aggression, have no social contact, which may mean we are not providing for their social needs; more research is needed.

Key resources

African Pygmy Hedgehogs- Care and Treatment Advice (Bament and Mancinelli, 2014)

African Pygmy Hedgehog Care (Hedley, 2011)

African Pygmy Hedgehogs (Johnson, 2010)

A retrospective study of disease incidence in African pygmy hedgehogs (Atelerix albiventris) (Okado et al., 2018).

1.2 Rodents

1.2.1. Chipmunks, Family Sciuridae

Invasive alien species legislation, prohibiting the keeping of Siberian chipmunks, Eutamias sibiricus, as pets, came into force in August 2016 in Europe (including the UK). Importing, breeding and selling these chipmunks as pets is prohibited, although those already in an owner’s possession could still be kept. The maximum recorded lifespan of E. sibiricus (in Japan) is 8.5 years and 12.5 years (CABI and EPPO, 2021) and breeding may still be occurring despite the ban. Therefore, it is likely there are still some pet E. sibiricus chipmunks in the UK, as well as Eastern chipmunks (T. striatus).

a) Transport and handling

Wild-caught and captive alpine chipmunks (Neotamias alpinus) showed a significant increase in faecal glucocorticoid response to handling, while lodgepole chipmunks (N. speciosus) did not show a similar glucocorticoid response. No behavioural measures of stress were recorded, therefore it is difficult to conclude whether these responses demonstrate differences in coping ability, or whether N. alpinus is more stressed by handling (Hammond, Palme and Lacey, 2015).

b) Behaviour

Siberian chipmunks are semi-arboreal squirrels, which also burrow for nesting. In a zoo exhibit (Thessaloniki, Greece), which contained a tree and various cage furniture, the available climbing supports were categorised as terrestrial, arboreal and unnatural (metal cage and poles), then by size, in a study of behaviour frequency and enclosure use (Youlatos et al., 2008). Chipmunks showed a preference for 8-10 cm horizontal supports and hardly used the vertical supports. Locomotion occurred on both terrestrial and 8-10 cm arboreal supports, whereas postural behaviour (clinging, sitting, standing) occurred mostly on 8-10 cm branches. Chipmunks leap less than other squirrels, with “low optimum take-off angles and adducted forelimbs”, which make them less suited to leaping long distances, compared to related species. Accelerometer measurement of activity levels in wild chipmunks was validated (Hammond et al., 2016) and this technique could be used to compare the activity of captive chipmunks to assess the adequacy of their husbandry in permitting natural behaviour.

c) Nutrition

A single animal case study was reported from Switzerland, describing urolithiasis of unknown cause (Kohutova and Jekl, 2021). Uroliths are often linked with dietary influence on urinary pH. Little is known about urolithiasis in chipmunks and the veterinarian’s opinion in this article suggests that commercially available diets for rodents may not be meeting the needs of pet chipmunks: “Although there are available commercial diets for squirrels, quality of these diets may be poor and insufficient on levels of protein and protein source (plant, insect or animal origin). The chipmunk was fed a diet for rats, which may not be satisfactory regarding chipmunk nutrition.”

The RSPCA website (RSPCA, 2022b)details an appropriate chipmunk diet as: “Up to 50% cereals (oats, wheat, barley, corn and millet sprays). You can also give unsalted nuts such as pine nuts. Small amounts of washed, chopped fruit and vegetables such as apples, pears, bananas, oranges, carrots, sweet potatoes, bean sprouts, and tomatoes”. The literature search did not find any evidence of nutritional problems in captive chipmunks other than by Kohutova and Jekl (2021).

1.2.2. Degu

Degus, Octodon degus, are used in research into Alzheimer’s disease. Unless relevant to degu welfare, experimental studies as models for human medicine were not included in this review.

a) Capture or breeding

Maternal care and stress responses were compared between recently-captured and captive-bred degus, and the effect of corticosteroid administration was measured (Bauer et al., 2016). Recently-caught mothers were less responsive to their pups than captive-bred degus, and cortisol administration resulted in lower weight offspring born to captive-bred mothers. This was a laboratory study on maternal stress, rather than a reflection of the conditions in which pet degus are caught or bred.

b) Behaviour

The risk to degu welfare in captivity of “inadequate opportunities for learning and satisfaction of cognitive needs” was only described in broad terms and not tested (McBride, 2017).

c) Nutrition

Degus were included in a behavioural review of “small prey species” (McBride, 2017). Potential welfare issues described as specific to degus include the risk of dietary monotony leading to satiety and consequent inadequate fibre consumption. The RSPCA website (RSPCA, 2022c) states their requirement for a high-fibre diet and good quality hay.

d) Health and disease

A review of common dental disorders in degus (Long, 2012) examined data submitted to the “Degutopia” website and global internet forum “Degu Information Group” between August 2003 and December 2010. Dental disease is the most common degu complaint presented to veterinarians, with around 60 % of clinical cases being acquired dental disease (Jekl, Hauptman and Knotek, 2011). 137 cases were identified and information was collated on diagnosis, outcome, sex and age of the degus. The most common complaint was molar malocclusion, which is a chronic and painful condition, with spurs irritating the inside of the cheeks and causing difficulty eating and abscessation. In an extreme case tooth elongation led to the patient to stop eating, become dehydrated, lose weight and have difficulty breathing, due to overgrown teeth invading the nasal cavity (Mans and Jekl, 2016). Owing to the data collection method, the actual prevalence and relation to diet is unknown, but dietary causes, such as lack of fibre, are likely to play an important role.

Two clinical studies focussed on reproductive health of degus, (Mancinelli et al., 2013) describes surgical intervention for a case of pregnancy failure (foetal death), and a study of captive-bred degus found that degu pups in breeding colonies (Britain) compared to wild pups (Chile) gained weight more quickly (2-3g/day over 14 days compared with 1-2g per day) (Long and Ebensperger, 2010).

According to the RSPCA website (RSPCA, 2022c), degus have a high risk of type two diabetes, which is linked with feeding a diet too high in sugar (e.g., diets formulated for chinchillas, rabbits and guinea pigs, which contain fruit or molasses). A laboratory study found that feeding degus high levels of fructose over 28 months resulted in insulin resistance, fatty liver and cognitive impairment, in a condition similar to diabetes mellitus, termed “Fructose-Induced Metabolic Syndrome-Like Condition” (Rivera et al., 2018).

1.2.3 Dwarf hamsters

The term “dwarf hamster” includes several species of hamsters sold as pets, including Roborovski’s dwarf hamster (Phodopus roborovskii), Campbell’s dwarf hamster (P. campbelli), Siberian dwarf hamsters (P. sungorus), Chinese dwarf hamsters (Cricetulus barabensis griseus or C. griseus).

a) Behaviour

Dwarf hamsters are sociable, but territorial and maternal aggression are part of the behavioural repertoire of dwarf hamsters (P. campbelli and P. sungorus), which has led to their use as models in neurobiological research into aggression and biparental care (e.g., (Gammie and Nelson, 2005; Vella et al., 2005). No studies were found on aggressive behaviour in the context of commercial breeding, transport, or private ownership. Dwarf hamsters were also included in the review by McBride (2017), but no specific behavioural issues were identified. P. sungorus was tested for consistent and correlated personality traits in laboratory behaviour tests (Kanda, Louon and Straley, 2012). Individual activity level was the most consistent individual trait, and correlation between activity level and boldness was positive in young animals, but negative in older animals. Individual differences in activity level were not altered, when given an exercise wheel in their home cage (Kanda et al., 2017). This personality difference should be accounted for when assessing the welfare of captive P. sungorus. Roborovski’s dwarf hamsters are more active than Siberian dwarf hamsters, which was described as “hyperactivity”. Supplementation with tyrosine for 10 days (consequently decreasing serotonin turnover in the brain) reduced home cage activity (Kabuki et al., 2011). This study was conducted under laboratory conditions (in barren cages), using hamsters as a model for ADHD, and the findings are not interpreted with respect to pet hamsters.

b) Housing requirements

The RSPCA website gives general guidance on keeping hamsters as pets (RSPCA, no date a), which cites (Calderone and Jacobs, 1999), demonstrating that dwarf hamsters have UV vision and can see well in twilight. This review did not find studies evaluating the effect of housing, bedding and environmental enrichment on pet dwarf hamster welfare, but information on paw injuries in Syrian hamsters, Mesocricetus auratus, demonstrating that pine bedding was more effective at avoiding paw wounds than beta chip substrate, may be transferrable (Beaulieu and Reebs, 2009).

c) Health and disease

In the Journal of Exotic Pet Medicine most search results were case reports of single animals:

• Uterine horn torsion in a pregnant hamster (Neves et al., 2019). This condition is not common in hamsters and is known to occur in other mammals. No husbandry or species-specific factors were identified as risk-factors.
• Bilateral Harderian gland abscesses (diagnosed at necropsy), with no other cases reported in hamsters (Zaffarano et al., 2015).
• Cutaneous botryomycosis, which was not amenable to surgical or antibiotic treatment and resulted in euthanasia (Grosset et al., 2014). This complex condition is rare and not specific to hamsters, nor is it known to be associated with any particular husbandry factors.
• Severe papillomatosis in P. sungorus, which resulted in euthanasia, but was previously unknown to occur in such a widespread, multifocal form in hamsters (Casanova et al., 2017), Spain.
• Neoplasia is common in rodents and case reports included treatment of squamous cell carcinoma (Martorell et al., 2005), surgical excision of a subcutaneous myxosarcoma (Wong et al., 2021) and anaplastic sarcoma of the cheek pouch (Rainwater et al., 2011), which was surgically excised, but later recurred.

A review of neoplasia in hamsters in Germany was recently undertaken (Rother et al., 2021), which included 177 hamsters which had been submitted to university facilities for necropsy. This useful guide to the most common tumours and survival time in hamsters does not represent a full view of the incidence of tumours in different species, since the submission rate of histopathology samples from all tumours that occur, and the number of pet hamsters in the population, is unknown.

1.2.4. Chinchillas

The long-tailed chinchilla (Chinchilla lanigera) is farmed for fur, as well as its use as a pet and in zoos. Infectious disease is reported here only where it occurs in captive animals and where the climactic conditions are similar to Scotland, since flora are likely to reflect local conditions. The RSPCA website provides advice to owners (RSPCA, 2022a).

a) Transport and handling

With gentle handling by experienced keepers, chinchillas can be trained to voluntarily step onto a person’s (gloved) hand and to enter a transport crate, but they are more alert and active in the presence of humans and not all chinchillas are receptive towards handling, requiring two or more attempts at catching (Baskir et al., 2020). The proportion of chinchillas, which accepted handling and carrying readily or resisted, was not quantified in this study.

b) Behaviour

Abnormal, repetitive behaviours in farmed chinchillas include, but are not limited to, fur-chewing (Ponzio et al., 2007; Franchi et al., 2016; González et al., 2018; Świȩcicka, 2018). This behavioural response to captivity is of financial importance to the fur industry and was therefore studied in this environment, but could indicate poor husbandry in pets.

c) Housing requirements

An investigation into the care of pet chinchillas in Germany found that 62.5% of the chinchillas are housed in cages that were too small (below minimum recommended) (Bläske et al., 2019). Key concerns in the welfare of pet chinchillas include the need to be kept socially with their own species, provision of adequate dietary fibre for gastrointestinal health and to avoid dental problems (Nikoletta et al., 2019). Preference testing demonstrated that chinchillas prefer to drink from open water dishes and they have a lower water requirement than guinea pigs and degus (Hagen et al., 2014)

d) Nutrition

Chinchillas are from arid climates and have a modest daily water intake of 2–12ml/ 100g body weight at ambient temperature. Chinchillas drink much more when fed on an exclusively hay diet (3.48 ± 1.31ml/g) than a mixed (1.17 ± 0.49) or pelleted diet (1.47 ± 0.49), so normal urinary output should be assessed in the light of what and how much the chinchilla is eating (Wolf et al., 2020).

e) Health and disease

A case report (Smith et al., 2010) described a 12-year-old chinchilla with a salivary gland carcinoma. (Crossley and del Mar Miguélez, 2001) demonstrated systematic dental abnormalities in pet chinchillas; cheek tooth lengths of clinically normal and captive bred animals with dental disease (average 7.4mm and 10mm respectively) were significantly elongated compared with wild-caught chinchillas (5.9mm average), which is attributable to an inappropriate diet. This study has not been replicated in the UK in the past two decades.

“Veterinary care of chinchillas” (Saunders, 2009) describes common problems of pet chinchillas, including fractures, fur slip, bite wounds, non-infectious conjunctivitis, matted fur, fur ring and paraphimosis, alopecia and fur chewing, heatstroke, heavy metal toxicity, electrocution, hyperthyroidism, diabetes mellitus (occasional) neoplasia (few reports), urinary tract disease (infrequent), gastrointestinal disorders and infectious diseases. The prevalence of these diseases is not reported, and the risks associated with conditions encountered during breeding, trade and keeping are not known. The prevalence of cardiopathy is unknown; a small study found that three of a group of 20 chinchillas had audible murmurs, (Linde et al., 2004).

Summary: Rodents

Guidance on the care of these rodents is available in veterinary literature and on the RSPCA website. The extent to which their specific nutritional, behavioural and other husbandry needs are being met by pet owners is not evident in the literature.

Chipmunks

Biological or behavioural needs which are difficult to provide in captivity.

• Chipmunks in captivity require an environment with horizontal branches, which gives them opportunities for climbing and leaping.

Evidence of harm associated with captivity.

• Wild chipmunks are stressed by human handling, but their response to humans when kept as pets is not published.

More information is needed to understand the welfare of this animal.

• The Siberian chipmunk now cannot be owned in the UK, so research should focus on the needs of other species, such as Tamias striatus.

Degus

Evidence of harm associated with captivity.

More information is needed to understand the welfare of this animal.

• Inappropriate diets are also likely to cause metabolic syndrome.

High prevalence of dental disease suggests captive degus are not receiving appropriate diets.

• The behavioural needs of pet degus and their provision are not known.

Dwarf hamsters

Biological or behavioural needs which are difficult to provide in captivity.

• High requirements for activity (especially at night).
• Social, but express territorial aggression.

Evidence of harm associated with captivity.

• Evidence of paw damage associated with inappropriate bedding and cage materials in Syrian hamsters may also affect dwarf hamsters.
• Dwarf hamsters may be predisposed towards neoplasia.

Chinchillas

Evidence of harm associated with captivity.

• Chinchillas are susceptible to dental disease, if not fed an optimum diet. Severe dental disease requires regular, invasive, surgical treatments.
• Chinchillas demonstrate fur-chewing as a response to poor environments.
• Chinchillas can be conditioned to voluntarily accept human handling.

More information is needed to understand the welfare of this animal.

• Breeding and keeping of hystricomorphs, such as the chinchilla, should focus on avoiding both congenital and acquired causes of dental malocclusion.

Key resources

Degus and chinchillas as laboratory animals and pets (Nikoletta et al., 2019).

Chipmunks (RSPCA, 2022)

Degus (RSPCA, 2022)

Hamster factfile (RSPCA, n.d.)

Chinchillas (RSPCA, 2022)

Veterinary care of chinchillas (Saunders, 2009)

Small prey species’ behaviour and welfare: implications for veterinary professionals (McBride, 2017)

1.3. Carnivores

The carnivores included in this review are: coatis, Nasua spp., leopard cats, Prionailurus spp., meerkats, Suricata suricatta, ocelots, Leopardus pardalis, and servals, Leptailurus serval. “Small nondomestic felids in veterinary practice” details the basic husbandry and care of the ocelot, as well as some hybrid species of non-domestic felids (Eckermann-Ross, 2014). The veterinary journal “Veterinary clinics of North America: Exotic Animal Practice” published an article on the nutrition and natural history of the serval and caracal, Caracal caracal (Livingston, 2009). The European Association of Zoos and Aquariums (EAZA) does not currently publish best practice guidelines for these species. The American Association of Zoos and Aquariums (AZA) published a “Minimum Husbandry Guidelines for Mammals: Small Felids”, (Mellen, 1997). Owing to the non-domesticated nature of these species, they may be subject to dangerous wild animal legislation (ocelot, leopard cat and serval) and therefore must be kept in a secure enclosure, rather than being considered house-pets. Minimum standards described in Mellen (1997) include:

• Enclosure sizes <10kg, 2 x 2 x 2.5m per cat, <20kg, 4 x 2 x 2.5m per cat, with further aerial pathways to encourage climbing. Platforms and hides, as well as logs to sharpen claws.
• Further basic guidelines are described on temperature, light, ventilation, water and sanitation, nutrition and vaccination. None of these requirements is sophisticated, except the instruction to “consider the regular use of a whole prey and/or bones with meat attached both for oral health and to stimulate natural eating behaviours”, which may pose hygiene challenges for the non-specialist keeper.

In the absence of species-specific literature, the search was widened to the welfare of small, zoo-housed felids and carnivores.

1.3.1. Coatis

Few studies on Web of Science mentioned coatis. One study reported phaeochromocytomas in two coatis (Reppas et al., 2001), neither of which were stated or suspected to relate to conditions relating to life in captivity or any factors relevant to this review. None of the other results had any relevance to domestic or pet coatis.

Only one individual was listed on an exotic pet license, issued from 2014-2018 by APHA (Elwin et al., 2020). In the “Journal of Exotic Pet Medicine” coatis only appeared in relation to advice on tranquilisation (Lennox, 2014).

The term “coati” yielded two case reviews, a case of arterial thromboembolism in a brown-nosed coati, Nasua nasua, in Singapore Zoo (Heng and Hsu, 2021) and one pet South American coati, N. nasua (in Denmark), with severe dilated cardiomyopathy, which may have been related to an inappropriate, protein-deficient diet (primarily breakfast cereals, small amounts of vegetables, raw chicken and shrimps) (Halck, 2021).

1.3.2. Leopard cats

There are two species of leopard cat; the mainland or Asian, Prionailurus bengalensis, and the Sunda leopard cat, P. javanensis. The Asian leopard cat is hybridised with domestic cats, Felis catus, to produce “Bengal” domestic cats. However, searching “Web of Science” did not yield any information on the breeding, transport, captive housing or welfare of leopard cats. 18 results for the term “leopard cat” were found with country/ region as Scotland, England, Wales or Ireland, but none of these studies related to animals being kept in the UK. A study on the handling of captive Prionailurus bengalensis euptilurus in Tchernogolvka, Russia, demonstrated an immediate significant increase in serum cortisol, 20 minutes after capture, and handling was associated with an initial decrease in red and white blood cells (Pavlova et al., 2018). Infectious diseases documented include FIV (Feline immunodeficiency virus) (Hayama et al., 2010), clonorchiasis (Choe et al., 2019) and ascarids (Xie et al., 2020), but all of these cases were found in Asia.

1.3.3. Meerkats

Meerkat, Suricata suricatta, studies were limited to the behavioural ecology of wild meerkats, which inform potential keepers about their normal social structures and social behaviour, but the Web of Science search did not find any evidence for the welfare impact of capture, breeding or life in captivity on behaviour or welfare.

A Pubmed search retrieved an additional article relevant to stress in captivity, comparing zoo populations of meerkats (Scott et al., 2017). Faecal glucocorticoid metabolites were used as an indicator of stress, and this welfare indicator demonstrated an increase in stress associated with contact with humans (greater visitor numbers) and living in small groups. Meerkats are being kept as pets in the UK as evidenced by sales websites, such as “ukclassifieds.co.uk”. Their social requirements for large group sizes and natural roaming, digging and scent marking render them unsuitable as household pets according to the RSPCA (RSPCA, 2022d).

1.3.4. Servals

a) Behaviour

Servals, Leptailurus serval, are solitary hunters in the wild, with a home range of 4 km² for females to 8 km² for males in the Ngorongoro Crater, Tanzania (Geertsema, 1984). Behavioural issues arising from lack of stimulation in captivity, as well as “undesirable” behaviours, such as frequent scent marking and disinclination to bury their faeces and therefore be litter-trained, are reported as issues in these “pet” animals. Their nutritional requirements are not known and therefore estimated based on their similarity to the domestic cat (Livingston, 2009).

b) Health and disease

In a study of ocular disease in captive, non-domestic felids (Nguyen et al., 2022), which included 30 servals, five animals had ocular abnormalities (16.7%), which was roughly equal to the prevalence within felids as a whole (16.3% prevalence over the 25-year period of the study). Corneal ulceration was the commonest ocular abnormality, which is also the case in domestic felids. However, cataracts were diagnosed more commonly than is seen in domestic cats, which may have been secondary to heritable abnormalities, ageing, trauma or nutritional deficiencies. These animals were at a rescue facility in the USA.

Cystinuria is reported as a welfare concern in captive servals in the USA (Cannizzo et al., 2017), with a prevalence of 27% from a survey of owners and institutions participating voluntarily in a screening programme. Feline panleucopaenia virus has been detected in captive servals in South Africa (Lane et al., 2016), during an outbreak which included several felid species (including captive ocelots). Although this demonstrates their capacity to carry this virus, it does not mean this is a risk to captive servals in the UK and vaccines used in domestic cats may be effective in reducing this risk.

1.3.5. Ocelots

The behaviour of captive ocelots, Leopardus pardalis, was described by (Suárez et al. (2017) in the context of visitor impacts on two individuals kept in zoological gardens in southern Spain. Findings indicate that visitor presence had a generally negative effect on diurnal behaviour; during zoo open days ocelots spent more time sleeping and less time walking. Ocelots displayed agonistic behaviour only when visitors were present and spent more time in retreat spaces and hiding places. However, during human presence, ocelots also spent less time performing stereotyped walking.

(Cameron-Beaumont et al. 2002) studied affiliative behaviour in small Felidae, via questionnaires sent to handlers in 71 zoos in the USA, UK and South Africa and concluded that the Ocelot Lineage (the phylogenetic clade including the ocelot and other small spotted South American cats) had the highest proportion of individuals showing affiliative behaviour and therefore may be preadapted to domestication. No other studies relating to welfare implications of keeping ocelots were described.

Summary: Carnivores

Biological or behavioural needs which are difficult to provide in captivity.

a) Wild carnivores cannot live with humans like a domestic cat or dog and are subject to “Dangerous Wild Animals” legislation, requiring a secure enclosure.

b) Small felids require aerial pathways, platforms, hides and logs.

c.) Servals and ocelots have home ranges of several kilometres in the wild.

Evidence of harm associated with captivity.

d.) Ocelots in zoos react to human presence with more agonistic behaviour (fighting) and hiding in retreat spaces, but they also performed less stereotypical behaviour, which may reflect vigilance towards humans.

e.) Captive servals are vulnerable to corneal ulceration, but its aetiology is unknown.

f.) Capture and handling are stressful for leopard cats, and being in close proximity to humans may cause chronic stress, although this needs more investigation.

More information is needed to understand the welfare of this animal.

g.) No information was found on the conditions and welfare of these selected pet carnivores kept in Scotland, including the breeding and importation of pet animals.

Key resources

The Nutrition and Natural History of the Serval (Felis serval) and Caracal (Caracal caracal) (Livingston, 2009)

https://www.rspca.org.uk/adviceandwelfare/pets/other/meerkats

Small Nondomestic Felids in Veterinary Practice (Eckermann-Ross, 2014)

AZA Minimum Husbandry Guidelines for Mammals: Small Felids (Mellen, 1997)

1.4. Primates

The keeping of primates as pets is sufficiently rare that they are often treated as a taxonomic group rather than at the species level (e.g., Soulsbury et al., 2009). There are legal restrictions on the importation of primates into the UK, including entry through an appropriate Border Control Post, health certification and a four-month quarantine period for rabies (APHA, 2022). The numbers and species of pet primates kept in the UK were not known, when reviewed (Soulsbury et al., 2009). A recent DEFRA call for evidence of primates kept as pets in England resulted in an estimate of 1,000-5,000 individuals being kept privately, with common marmosets, Callithrix jacchus, being the most prevalent (DEFRA, 2020). However, the true number is unknown, nor is the degree to which primates are being kept in “zoo-like conditions” or as house pets. The DEFRA call for evidence did not reach any individuals keeping primates as pets, but Table 2 of the report summarises a range of physical and psychological issues experienced by primates kept in unsuitable conditions from case studies and academic research.

The removal of teeth and claws is mentioned as not advisable and/or illegal in husbandry advice (Wissman, 2014), suggesting that these are practiced (at least where the author’s clinical experience is based in the USA), although no published evidence of this was found. The AVMA has a policy of opposing the removal or reduction of healthy teeth from non-human primates and carnivores kept as pets (avma.org/resources-tools/avma-policies/removal-or-reduction-teeth-nonhuman-primates-and-carnivores). Primates without teeth are relinquished to facilities, such as “primate rescue centres”, but figures on the prevalence of this practice are not published. Johnson-Delaney (2008) describes biting as part of the normal dominance signalling by non-human primates, and advises vets that “monkeys bite, they bite quickly and hard, and they will always bite, even if their owners swear they do not”. Tooth-brushing, regular dental cleaning and chew toys, coated with sodium hexametaphosphate are recommended aspects of preventative dental care (Johnson-Delaney, 2008).

The social needs of primate species are crucial to their welfare. The “Code of Practice for Privately Owned Primates (DEFRA, 2010) states: “With few exceptions, they live in complex societies that can comprise tens of individual animals.” The early life period is also highlighted as important for the development and welfare of primates, which makes them remarkable among species typically regarded as suitable pets: “In relation to their total life history, primates have long infant and juvenile phases, with social independence occurring long after nutritional weaning”. The code of practice goes on to describe welfare-assessment methods available to owners of primates and requires keepers to be “registered with a veterinary practice that has specialist knowledge of the species kept”. Marmosets and tamarins, Family Callitrichidae, although not considered a danger to humans “cannot be considered pets, and require specialised knowledge, ownership should be preceded by hands-on experience with primates, and breeding should not occur unless offspring can be placed with owners able to provide suitable care”. Detailed guidance is given for what the behaviour of primates should look like (avoiding excessive aggression, appropriate sleeping and resting patterns, low anxiety around food, a wide range of foraging behaviours, appropriate defence and escape behaviours, a full range of physical activities, etc.).

The AZA provides a care manual for lemurs (Eulemur spp.) (Campbell et al., 2013), which represents a compilation of current knowledge provided by a variety of experts in the genus. Although publicly available, the document “is intended solely for the education and training of zoo and aquarium personnel at AZA-accredited institutions”. The USDA (United States Department of Agriculture) provides animal care aids (practical information is presented in simple language in an A4 poster format) on various aspects of primate care relevant to private keeping of primates, in particular their social needs, providing appropriate enrichment, rearing infants and juveniles and dealing with psychological distress.

While the current review focusses on the behaviour and welfare associated with keeping exotic animals as pets, it should be noted that the illegal pet trade directly threatens the wild population of lemurs in Madagascar (LaFleur et al., 2017).

Many species (including marmosets and tamarins) do not require dangerous wild animal licenses and compliance with dangerous wild animal licensing is reported to be low, although this information is not recent (Greenwood et al., 2001). There is strong objection by veterinary organisations to keeping primates as pets: “We can think of no circumstances where a primate would benefit from being kept privately as a pet. They are unsuitable to be kept as companion animals.” British Veterinary Association and British Veterinary Zoological Society” (BVA and BVZS, 2020).

1.4.1. Bushbabies

a) Transport and handling

Relocation stress has been studied in northern greater bushbaby, Otolemur garnettii, (Watson et al., 2005) in the context of a planned relocation between universities 90 miles apart (by road). The home cages were relocated into the new environment and cage-mates were kept together. On the day of relocation a near ten-fold increase in cortisol from baseline was observed. Faecal cortisol had returned to normal when the next sample was taken at seven days after moving.

a) Behaviour

The Senegal bushbaby, Galago senegalensis, is nocturnal primate, known to vocalise frequently. Schneiderová et al. (2016) studied vocalisations of lesser galagos, G. senegalensis, and reported regular attention/ alarm calls. Loud vocalisations were infrequent, but “could be emitted repeatedly in long series lasting for several minutes”. Alarm vocalisations increase in captive conditions and are associated with environmental and social disturbances (Zimmermann, 1989; Boinski et al., 1999). Bushbabies increase production of loud calls before and at dawn (Schneiderová et al., 2016). Self-injury, which may reflect redirected or thwarted aggression, is commonly reported in captive non-human primates.

Bushbabies also exhibit stereotypies. In a university laboratory primate facility (Jackson State University Center for Prosimian Studies) a study of 22 northern greater bushbabies (Otolemur garnettii) exhibiting self-injurious behaviour compared with 11 control animals demonstrated a positive effect of daily L-tryptophan treatment on self-injury and stereotyped behaviours (McCoy et al., 2009) However, bushbabies exhibiting self-injury did not have significantly lower baseline serotonin than control animals, demonstrating the harmful behaviour is likely to be a response to circumstances rather than individual differences in neurophysiology. Classical music was tested as a form of auditory enrichment for eight O. garnettii (Hanbury et al., 2009), which were exhibiting stereotypic behaviour in a laboratory colony of bushbabies, University of Southern Mississippi. The music did not influence either stereotypy or grooming behaviours. Bushbabies experience handling stress, even when caught and restrained regularly by experienced animal handlers. In a study at the University of Mississippi, the use of food reinforcement was not successful in reducing the negative emotional response to restraint, which was reflected by increased tympanic membrane temperature (Hanbury et al., 2013).

c) Housing requirements

Bushbabies are arboreal (Rosenson, 1972) and require branches to climb. In a study of environmental enrichment for Galago senegalensis at Paignton Zoo Environmental Park (Clark and Melfi, 2012), artificial termite mounds and gum feeders were successful in encouraging species-typical behaviours, although bushbabies also responded to auditory stimuli (rainforest sounds) by moving away into the nest boxes, which may indicate neophobia (fearful of sounds that were not familiar, despite their ecological relevance). Like all bushbabies, Moholi bushbabies, G. moholi. are nocturnal (Rosenson, 1972) and while they should ideally not be disturbed during the day, in a zoo exhibit they were substantially more active when housed under red lighting than blue lighting. However, only two individuals were tested and the female bushbaby gave birth during the experiment (Fuller et al., 2016). It is possible that inappropriate levels of blue light will have detrimental welfare effects on captive bushbabies, but further research is needed to establish ideal lighting conditions.

d) Nutrition

A study of nutrient intake and availability in 11 captive O. garnettii established that an insectivorous diet had higher non-digestible fibre, crude protein and dry matter digestibility to a frugivorous diet (Smith et al., 2020). Diet has been studied from an anthropological viewpoint rather than assessment of the nutritional adequacy of diets provided to privately owned bushbabies.

e) Health and disease

The search elicited few studies of disease in bushbabies. An article in “Microbiology society” journal reported that an isolate of Pasteurella B species (as found in dog and cat bites) was found in a Moholi bushbaby, Galago moholi, at Copenhagen Zoo (Christensen et al., 2012). A single case report of a fibroepithelial tumour, called “Phyllodes-like” mammary tumour, was diagnosed after euthanasia of an 11-year-old captive northern greater galago O. garnettii (Jones et al., 2016).

f) Mortality

Debyser (1995) reviewed prosimian juvenile mortality (from conception until weaning) in zoo and research populations from articles published during the period 1972- 1992. Mortality of G. senegalensis is estimated as 28-28.6% (captive population) and of G. moholi as 25.3- 61.6%. These figures are based on data from 1982-1900 (table III, Debyser, 1995).

1.4.2. Capuchin monkeys

EAZA produces “best practice guidelines” for keeping captive capuchins (Souvignet et al., 2019). There are two different subfamilies in the Family Cebidae, the squirrel monkeys (Saimirinae) and the capuchins (Cebinae). According to the RSPCA, the commonest captive capuchins in the UK are the black-capped or tufted capuchins, Sapajus apella. Capuchins are subject to “dangerous wild animal” legislation.

a) Transport and handling

In laboratory and zoo-housed capuchins, negative associations with routine husbandry procedures, including space restriction, can create stress and fear, which in turn can lead to the expression of stereotypic behaviour (de la Barrera Cardozo et al., 2021). Therefore, using positive reinforcement training can allow capuchins to associate tasks, such as moving to a crate with a reward, thereby increasing predictability and reducing stress (Brando et al., 2021).

b) Behaviour

Capuchins are diurnal and live in family groups in the wild, including “Single-male or age-graded group of 10-20 individuals. The Margarita Island capuchin groups (S. apella) are smaller: 4-6 individuals.” (Souvignet et al., 2019). Capuchins with a more sociable and active personality may be more resilient to stressful experiences, such as relocation, measured in terms of faecal glucocorticoid metabolites (Ferreira et al., 2020). In common with other primate species, the social needs of this species are challenging to meet. “Capuchins need to be kept in groups, however their social structure results in eventual evictions of group members. Therefore, keeping those animals implies having sufficient enclosures to accommodate evicted animals in appropriate conditions.” (Souvignet et al., 2019).

c) Nutrition

Capuchins are frugivore-insectivores (Mittermeier et al., 2013). Energy is provided by the fruits and the proteins are provided by small animal prey (insects).

d) Health and disease

Infectious diseases have been studied in the context of captive capuchin monkeys in Ecuador (gastrointestinal parasites; (Martin-Solano et al., 2017) and Brazil (trypanosomatids; (Aysanoa et al., 2017), but parasitic burdens are highly specific to climate and location and we cannot use these studies to infer disease or health status of the UK population of captive and/ or pet capuchins. No data are available on welfare in transport, although a single study advertised a transport cart cage for laboratory use (Lowery et al., 2001).

1.4.3. Lemurs

Lemur species kept commonly as pets include ring-tailed lemur, Lemur catta, black-and-white ruffed lemur, Varecia variegata and brown lemur, Eulemur fulvus. Dangerous wild animal licenses are required for i) Indriidae (“leaping lemurs”), including the indri, Indris indris, sifakas, Propithecus spp., and woolly lemurs, Avahi spp. and ii) Lemuridae (except the gentle lemurs, Hapalemur spp. and the broad-nosed gentle lemur, Prolemur simus).

a) Transport and handling

A single study on transport stress was found (Volfová et al., 2019). Two female black-and-white ruffed lemurs, Varecia variegata, were transported 202 km between zoos in individual transport crates. This form of transport can be considered a mild stressor, with a decrease in some forms of comfort behaviour in the new environment compared to pre-transport (sunning, scratching, stretching and allogrooming) and an increase in faecal glucocorticoid metabolites, which was evident two days after transport.

b) Behaviour

Aggression within lemur groups is a topic of interest for ethologists (Roeder, Duval and Gosset, 2002), particularly because lemurs in the wild and in captivity perform post-conflict affiliation and in some cases reconciliation (Colmenares, 2006; Palagi and Norscia, 2015). From a welfare perspective, aggression is part of the behavioural repertoire of captive lemurs, and owners need to correctly treat bite wounds. A recent study of ring-tailed lemurs from five British zoos evaluated bite-wound management in lemurs (n=88) living in troops of 10 or more (Ceccolini et al., 2021). Over the study period (2015-2019), 211 bite wounds were observed and 51 required surgical treatment. When presented with a food source within a marked area, red-fronted lemurs, Eulemur rufus, were more socially tolerant than ring-tailed lemurs (Fichtel et al., 2018), and captive lemurs were more likely to tolerate others feeding at the same time than their wild counterparts, but total rates of aggression were not impacted either by species or by setting.

The behaviour of free-roaming, captive-born and mother-reared ring-tailed lemurs, Lemur catta, at Fota Wildlife Park, Ireland was largely unaffected by the presence and number of visitors. They chose to interact infrequently with visitors (this was observed during 1.03% of observations), and rarely reciprocated when visitors tried to feed, frighten, or approach them. Their overwhelming response, to ignore humans’ attempts at interactions, suggest that unfamiliar humans are not regarded as socially relevant to lemurs, but that in this environment they are able to habituate to human presence. When visitors were present at feeding times (crowned lemurs, Eulemur coronatus) in Newquay Zoo (Jones et al., 2016), the lemurs performed significantly less aggression, compared with feeding occasions when only the keeper was present. The implications for pet ownership are not clear; lemurs gradually increased their attention towards visitors over time, which may show an initial wariness followed by desensitisation, so lemurs explored visitors once they were used to being fed in their presence.

38 ring-tailed lemurs at Duke Lemur Center (USA) were assessed for “allostatic load”, using biomarkers to estimate the level of chronic stress they experienced in captivity (all the lemurs were over one year old at the time of sampling). Increased time spent indoors, and living in a small group both increased allostatic load, suggesting these factors have a significant, negative influence on welfare (Seeley et al., 2021). An increase in faecal glucocorticoid metabolites was observed in captive black-and-white ruffed lemurs, Varecia variegata, when the level of disturbance exceeded that associated with daily husbandry, e.g., relocation (involving handling and capture), or construction work near to their enclosure (Volfova et al., 2020).

Lemurs are highly curious and are attracted to novel objects. Feeder enrichments are common and effective in increasing the amount of time spent performing behaviours observed in the wild. For example, whole rather than chopped food increases the time spent feeding (Kerridge, 2005) and presenting food which requires lemurs to manipulate containers increases simulated foraging and general activity (Sommerfeld et al., 2006; Dishman et al., 2009; Shapiro et al., 2018; Fernandez and Timberlake, 2019). Different types of feeder design are more suited to different lemur species. Shapiro et al. (2018) tested three types of enrichment and concluded that the “bottle feeder” was most engaging for ring-tailed lemurs, whereas a “hanger” was more appealing for red ruffed lemurs, Varecia rubra, whereas Coquerel's sifaka, Propithecus coquereli, used both types of enrichment more than the food bowl, but had no preference between the two. Positive reinforcement training, carried out at “Parco Natura Viva”, Italy by animal trainers, following a structured habituation and training programme, resulted in decreased aggressive and increased affiliative social interactions (Spiezio et al., 2017).

c) Housing requirements

No studies compared the effect of enclosure size on lemur welfare, but there were zoo studies on environmental enrichment. As lemurs are highly arboreal, branches for climbing should be provided, which need to be cleaned and varied regularly. Aerial nest-boxes have been used in zoos (Campbell et al., 2013). Although Baker et al. (2018) found that a range of new smells (lavender, peppermint, coconut, and morio worms, Zophobas morio) added to an enclosure had a generally stimulatory effect on activity as well as resting behaviour, there was no significant difference between the type of odour presented. In contrast, a trial at Dudley Zoo (Vaglio et al., 2021) found that the use of oils (benzoin, lavender, lemongrass) as a putative “enrichment” resulted in a significant decrease in social behaviour and increase in faecal glucocorticoid levels in captive red ruffed lemurs. This suggests that lemurs are sensitive to different types of scent, and care is needed to avoid inadvertent negative effects on welfare by introducing new scents.

The natural habitat of lemurs (Madagascar) is warmer than Scotland, with an annual mean minimum and maximum temperatures of 12.4–34.2 °C (Sha et al., 2020), compared to Scotland (average mean minimum and maximum approximately 5-15°C). In a study of primates at Guangzhou Zoo (lowest mean temperature 9.9°C), lower temperatures were not associated with a change in activity levels in ring-tailed lemurs, but this species dedicated most time to thermoregulation behaviour (sitting hunched, or huddling with others). However, in response to food scarcity in the wild, reduced activity, torpor and hibernation are part of the normal behavioural repertoire of mouse and dwarf lemurs, Family Cheirogaleidae (e.g., Goodman’s mouse lemur, Microcebus lehilahytsara (Karanewsky et al., 2015)). This winter hibernation is still expressed in the zoo environment and during this time the lemurs sleep in same-sex groups (Karanewsky et al., 2015). Fat-tailed dwarf lemurs, Cheirogaleus medius, hibernate 3-7 months per year in the wild and will enter a state of torpor when husbandry conditions are adjusted so that it is cooler (10-15°C) and food is restricted (Blanco et al., 2021). AZA guidance states: “When temperatures fall below 18.3 °C (65 °F) heat sources (as described below) should be provided. When temperatures fall below 8.9 °C (48 °F), animals should be housed indoors only.” The provision of shelter and heat sources that are sufficient for all animals to have access regardless of their social status, ventilation and back-up systems in case of faults with the buildings, are described. However, in agreement with the lack of information on lighting found in this review, “little research has been conducted on the light intensity requirements of Eulemur species. Some Eulemur holding institutions report the use of UVB light bulbs or vita-lights to supplement exhibit lighting, particularly in the case of animals housed without access to natural lighting. More research is needed in this area.”

d) Nutrition

Lemurs are frugivorous and, when given the choice, will select foods which are high in carbohydrate and in particular sucrose (Fernandez and Timberlake, 2019; Hansell et al., 2020). The diet of these primates in captivity often affects gut microbiota negatively, due to the feeding of plants selected for higher sugar content and lower fibre than would be encountered in the wild. Supplementation of romaine lettuce resulted in enrichment of microbial populations associated with fibre digestion, and increased foraging behaviour (Greene et al., 2020). Across 13 European zoos body weights of ruffed lemurs, V. variegata, were significantly higher than wild populations, and 46.5% of captive individuals were categorised as obsese (Schwitzer and Kaumanns, 2001). Obesity may reduce life-span. In contrast, chronic calorie restriction in grey mouse lemurs, Microcebus murinus, (on average 71kJ/day compared with 105kJ/day in controls) was reported to extend lifespan (initial results showed an increase of 22% in lifespan, (Pifferi et al., 2018), but there was also an associated accelerated loss of cerebral grey matter.

Lemurs can progressively accumulate iron in their digestive organs, which can result in toxic effects on the liver and premature death (Andrews et al., 2005). Prevalence of iron storage disorders vary across lemur species, with a lower prevalence in L. catta (16.7% haemosiderin-positive on necropsy) compared with other species such as Varecia variegata (50% positive) and Eulemur coronatus (57.1% positive) (Wood et al., 2003; Glenn et al., 2006). Dietary interventions (increased vitamin C, reduced iron and increased tannins) have been shown, using transferrin saturation tests, to reduce iron serum levels (Wood et al., 2003).

e) Health and disease

The diet of captive lemurs is likely to be an important factor in the rate of tooth wear, which in turn affects welfare and mortality. Although these variables were not systematically compared, two populations of zoo lemurs were studied and those which had annual veterinary and dental examinations, tooth cleanings and more varied and fibrous, “leaf-eater” diets (Indianapolis Zoo), had much lower levels of dental wear than lemurs with less veterinary intervention, and which were predominantly fed on tamarind fruits (at the Bezá Mahafaly Special Reserve in Madagascar BMSR) (Cuozzo et al., 2010). Compared with grey mouse lemurs in the wild, those in a captive setting (a breeding colony, housed in a cage measuring 2m³ and containing three plastic tubes and three nesting boxes, (Némoz-Bertholet et al., 2004), had weaker grip strength and began to decline in strength at a younger age than wild lemurs (Hämäläinen et al., 2015).

Studies of infectious disease existed mostly for wild populations in Madagascar (Spencer and Irwin, 2020). In relation to captive ring-tailed lemurs (L. catta), there is evidence they can become infected with Echinococcus multiocularis, spread to wildlife parks by foxes, Vulpes vulpes (Umhang et al., 2013). Five cases of E. multiocularis, including one animal which had alveolar echinococcus diagnosed at necropsy, detected in at Parc Animalier de Sainte-Croix in France demonstrate the potential for L. catta to host this parasite and therefore pose a serious risk to human and animal health. Therefore, routine anthelmintic treatment (as in pet dogs and cats) is necessary for lemurs in close contact with humans, but there have been no cases of domestically acquired cases of E. multiocularis in the UK (https://www.gov.uk/guidance/echinococcus-multilocularis-how-to-spot-and-report-the-disease). Widespread use of antibiotics in Madagascar has affected the abundance of anti-biotic resistance genes in wild lemurs (Bornbusch and Drea, 2021). Resistance is present even in wild populations with little human disturbance, but in captive lemurs the antibiotic resistance genome was considerably enriched. These captive animals were housed either in LRC (Lemur Rescue Centre, Madagascar) or DLC (Duke Lemur Centre, United States) and the type of resistance found depended on the most commonly used antibiotics in the respective countries. In a case study of an illegally owned pet ring-tailed lemur in Madagascar, streptomycin-resistant M. tuberculosis was isolated (LaFleur et al., 2021).

f) Mortality

In Coquerel’s sifakas, Propithecus coquereli, housed at the Duke Lemur Center (1990-2015), the median age of death in animals that lived longer than 30 days is 10.3 years and the most common causes of deaths were stillbirths (64.7% of deaths in the perinatal group), enteritis-colitis, failure to thrive (in the perinatal period) and protozoal infections (Cassady et al., 2018). Even where breeding programmes are managed in order to retain genetic diversity, breeding colonies show genome-wide inbreeding effects. Homozygosity makes L. catta more vulnerable to disease, in particular parasitism, and more likely to die prematurely, compared to more heterozygous individuals (Charpentier et al., 2008).

1.2.4. Marmosets

Marmosets belong to three genera: Callithrix spp., Mico spp. and Cebuella spp. According to the RSPCA report “Do you give a Monkey’s?” (RSPCA, 2016), marmosets are the most commonly kept primate in the UK, comprising chiefly common marmosets, Callithrix jacchus, Geoffroy’s marmosets, C. geoffroyi, and their hybrids. EAZA publish best practice husbandry guidelines for the Callitrichidae (Ruivo and Stevenson, 2017). This taxonomic group include 61 species and subspecies: 22 marmosets, Callithrix spp., Mico spp. and Cebuella spp., 34 tamarins, Saguinus spp. and Leontocebus spp., four lion tamarins, Leontopithecus spp., and Goeldi’s monkey, Callimico goeldii. Common marmosets in the wild live in scrub, swamps and tree plantations. Infants are weaned at two months old and reach sexual maturity at 12 months old for females and 16 months old for males. Their most active period is early morning and late evening (Ruivo and Stevenson, 2017).

A key health consideration relevant to human contact with marmosets and tamarins, is that herpes simplex virus, highly prevalent in the human population, is fatal to callitrichids (Ruivo and Stevenson, 2017). In addition, mice can carry viruses, which cause lymphocytic choriomeningitis (callitrichid hepatitis), therefore feeding “pinkies” or exposure to wild mice, Mus musculus, is not recommended (Ruivo and Stevenson, 2017).

a) Breeding

In laboratory-bred marmosets humans may have to intervene to supplement feeding, which is disturbing for the mother. Handfeeding of triplet offspring did not affect cortisol or behaviour changes in response to a stressful procedure (capture, handling, weighing and release into a new clean cage). However, this procedure increased agitated locomotion (Ash, Smith and Buchanan-Smith, 2021). The management of dystocia using techniques, such as the use of oxytocin or forceps, often leads to complications and so timely use of caesarean section is recommended (Ruivo and Stevenson, 2017). This highlights the importance of liaising with specialist veterinarians before any planned breeding. Detailed instructions on the hand-rearing of callitrichids is published in veterinary journals and available at: www.exoticpetvet.net/primate/callitrichid.html. This is based on the expertise and experience of a veterinary surgeon (Wissman, 1999), an avian/exotic specialist vet, who co-owns a sanctuary for marmosets and tamarins. Data are not presented about the success of breeding marmosets and tamarins in domestic settings (i.e., outside zoos). The issues raised include potential for rejection, trauma and even cannibalism of offspring by inexperienced parents. Where marmosets are reared without their parents, there is a need for intensive and specific feeding and infant-carrying by owners acting as “substitute” parents. The tendency for callitrichids to give birth at night increases the risk of owners missing dystocia cases. Short intervals between births increases the risk of infant mortality (Frye et al., 2022).

b) Transport and handling

Moves between exhibits in the same building, between indoor exhibit buildings and between all zoo buildings were analysed for their effect on weight in captive callitrichids (Kaplan and Shelmidine, 2010). In marmosets, relocation was associated with at least 5% weight loss in 44% of cases and more rarely weight gain (6%). Similar figures were observed for tamarins, with 35% of housing events resulting in a 5% weight loss or greater, and 6% with weight gain.

c) Behaviour

Marmosets and tamarins in zoos may be hand-reared, but are still nervous and handling is not recommended. Stress associated with restraint can even lead to death during or just after capture (Ruivo and Stevenson, 2017). Keepers are advised to maintain “neutral relationships” to reduce fear in animals, when capture is necessary, and the effect of their distress on others in the social group. Bites to human handlers can be deep, and teeth can be damaged if handling is rough, e.g., pulling away from the marmoset if it bites into a glove during restraint. A lack of hiding areas with reduced visibility to visitors is a risk factor for developing marmoset wasting syndrome (Cabana et al., 2018).

The welfare of non-breeding females kept in single-sex groups may be negatively affected by the restriction of their behavioural repertoire. Rearing young is an important part of social life, and therefore euthanasia of surplus offspring may be carried out in zoos. The justification for this is related to exhibiting zoo animals in conditions that reflect their true behaviour to the public. Greater understanding of the costs and benefits of breeding, particularly for females, is an important avenue for future research. Multiple births are more usual than single births, and twins increase the risk of neonatal mortality. In zoos, larger litter sizes (often triplets) are more common than in the wild, because nutrients are more easily available. Neonatal mortality (death before 30 days of age) was multifactorial, and included birth problems, poor maternal care and infectious disease. Rearing of infants by several members of the social group (helpers) may be an important factor in infant survival (Anderson and Dennis, 2018) and participation in caring for younger siblings is a means of learning about parental care.

d) Housing requirements

EAZA best practice guidelines are available for housing standards in zoos (Ruivo and Stevenson, 2017), including a recommendation to allow outdoor access, to provide minimum humidity of 60% and an indoor temperature of 18 ^oC, natural substrates, nest boxes, nesting material, ropes and plants. A list of toxic and non-toxic plants is included.

e) Nutrition

Marmosets are morphologically adapted to eating plant exudates and in the wild are found in forests in the Neotropical region of South America. Pygmy marmosets, Cebuella spp., are particularly specialised for gouging plants in order to produce exudates, and their diet is primarily exudate, insects and spiders. Callithrix jacchus is highly exudativorous, and C. geoffroyi is less reliant on exudates than C. jacchus, but is still well adapted for tree gouging. Gums are a poor source of energy, but important for the provision of calcium, magnesium, potassium and iron (Ushida et al., 2006). A review of the nutritional management of marmosets in seventeen research colonies found that gastrointestinal disease was the most common clinical illness and obesity was common (on average 20% of the institute’s population). The report is related to the diet of experimental animals and one of the concerns is that captive diets may be unnecessarily varied, which is not a concern for pets. The overall finding is that clinical illness is likely to relate to poor diet, but there is a lack of evidence to inform the ideal marmoset diet. The authors summarise the state of knowledge on marmoset nutritional management as reliant on “anecdotal or historical precedence, animal food preferences, or published reports that focus on the role of a limited number of very specific diet components in relatively small numbers of animals”.

Laboratory marmosets are fed either once (59% of institutions) or twice (41%) daily, with additional treats used for training. A base diet is provided, with fruit as supplemental food, most also use protein sources, vegetables and/or grains, 42% use dairy products and 18% use Arabic gum as enrichment or as a reward, which provides an important source of calcium. Food deprivation (inadvertently feeding marmosets either three hours or six hours after their normal feeding time) resulted in significant increases in serum cortisol and an increase in body temperature (tympanic membrane temperature) (Pereira et al., 2020).

1.4.5. Tamarins

Tamarins belong to two genera: Saguinus spp. and Leontocebus spp. The EAZA best practice guidelines (Ruivo and Stevenson, 2017) provide a rich source of information on the care and behaviour of tamarins.

a) Behaviour

Social groups are composed of several females and males, usually with a single breeding female. Tamarins are arboreal and diurnal, and their communication is based on vocalisations and scent marking. Their foraging behaviour is well described (Ruivo and Stevenson, 2017) and appropriate enrichment for zoo-housed tamarins has been studied (Franks et al., 2013). In zoo tamarins, feeding insects (mealworms) increased time spent climbing compared with fruit (raisins) and a puzzle feeder was effective in increasing foraging time and general activity (Sanders and Fernandez, 2020).

b) Housing requirements

Free-ranging tamarins are more active, whereas those socially housed in cages express more affiliative and agonistic behaviour. At Jersey Zoo the “caged” treatment consisted of male-female pairs, which had access at all times to indoor sheds (either 3.7 m² × 2.2 m or 7.2 m² × 2.4 m) and outdoor spaces (40 m² × 4 m high or 14.5 m² × 3 m high). Leaping and running are more often observed in the free-ranging tamarins, suggesting these are curtailed when there is not enough space.

c) Nutrition

Tamarins and lion tamarins (Leontopithecus spp.) feed on fruit and insects, with small amounts of flowers, other invertebrates and small vertebrates and fungi. In contrast to marmosets, they are not adapted to gouging plants for exudates and these constitute a smaller part of their diet. Tamarins rely on natural sources of exudates or steal from the gouges made by marmosets.

d) Health and disease

Urinary neopterin is a candidate biomarker predicting poor survival, which could be used as a non-invasive welfare measure in marmosets and tamarins (Sacco et al., 2020). The natural diet of tamarins and marmosets does not include gluten, but it is sometimes included in captive diets and is associated with gastrointestinal disease such as “wasting marmoset syndrome” (similar to human coeliac disease (Cabana et al., 2018).

e) Mortality

Neonatal mortality of tamarins at Cleveland Metroparks Zoo from 1990 to 2014 was 48.9% for Geoffroy’s tamarins (Saguinus geoffroyi), 45.9% for golden lion tamarins (Leontopithecus rosalia) and 59.3% for pied tamarins (Saguinus bicolor) (Anderson and Dennis, 2018). Factors relating to the complex requirements for parental care are discussed in the general introduction. In adult tamarins, colitis and enteritis are leading causes of mortality, and may be related to suboptimal temperatures, parasitism, stress and dietary inadequacy, although more research is needed to confirm this.

1.4.6. Squirrel monkeys

The Web of Science search found no publications referring to the welfare of pet squirrel monkeys, Saimiri spp.

a) Breeding

Squirrel monkeys reared with and without their mother showed significant differences in behaviour. Nursery-reared monkeys were less active and attentive and had slower motor development than those reared by their mother. Behaviour was analysed at two and six weeks old only (Bahia et al., 2011).

b) Behaviour

Squirrel monkeys readily participated in voluntary positive reinforcement training (clicker training) in a zoo environment. This technique can be used to reduce the stress associated with routine procedures, even intramuscular injections (Gillis et al., 2012).

Dominance structure is characterised by a linear relationship between the dominant (large) male and the rest of the social group ranked below him. Between lower ranked animals, differences in dominance and aggression are much less marked and several animals can occupy the same rank (Pinheiro and Lopes, 2018). In mixed-species groups, squirrel monkeys are less aggressive than capuchins. Enclosure design can improve affiliative and reduce aggressive encounters between individuals of different species (Buchanan-Smith et al., 2013). Changing the distribution of food can alter the dominance structure of a group (Bashaw, McIntyre and Salenetri, 2011).

Unwanted attention by juveniles of their own species (play invitations) causes chronic raised cortisol levels in adults, (Soltis et al., 2003). Housing conditions (particularly isolation or pair housing) can be a greater influence on behaviour than enrichment. Several studies have presented enrichment to squirrel monkeys, but not observed a reduction in stereotypy (Spring et al., 1997; Fekete et al., 2000).

c) Nutrition

Squirrel monkeys consistently prefer food with a higher energy content (Laska, 2001), which may negatively influence health if food presentation is not tailored to ensure they consume a complete diet.

d) Health and disease

Squirrel monkeys are susceptible to toxoplasmosis, which can be fatal (Nishimura et al., 2019; Carme et al., 2009). No studies were found to suggest a high susceptibility to diseases associated with captivity.

Summary: Primates

Bushbabies

Biological or behavioural needs which are difficult to provide in captivity.

• Bushbabies exhibit a strong stress response to handling and relocation.
• Require a complex, arboreal environment, may exhibit neophobia (in zoos).
• Frequent vocalisations, especially before and at dawn, loud alarm calls.

Evidence of harm associated with captivity.

• Stereotypic behaviour and self-injury indicate distress in captivity.

Capuchin monkeys

Biological or behavioural needs which are difficult to provide in captivity.

• Live in large family groups, from which evictions can occur.

Evidence of harm associated with captivity.

• Routine husbandry procedures in captivity can cause stress and fear.

Lemurs

Biological or behavioural needs which are difficult to provide in captivity.

• Arboreal and need branches to climb on, which can cleaned and varied.
• Adapted to a warm climate and natural sunlight (require UVB).
• Social and use biting as a means of resolving disputes.

Evidence of harm associated with captivity.

• Living in small groups and living indoors increases chronic stress.

Marmosets

Biological or behavioural needs which are difficult to provide in captivity.

• Breeding is high-risk; multiple births and may require caesarean sections.
• Handling is stressful for marmosets in zoos and chronic exposure to humans, without hiding places, contributes to the debilitating “marmoset wasting syndrome”.

Evidence of harm associated with captivity.

• Gastrointestinal disease and obesity are common in laboratory marmosets.

More information is needed to understand the welfare of this animal.

More information is needed to understand the welfare of this animal.

• Optimum diets are not well understood and may require plant exudates.

The welfare impact of not being able to express parenting behaviour is unknown.

Tamarins

Biological or behavioural needs which are difficult to provide in captivity.

• Normal behaviour of free-ranging tamarins includes running and leaping, which are curtailed when space is restricted even in zoo enclosures.
• Infant care is complex, with high levels of juvenile mortality in a zoo population

Evidence of harm associated with captivity.

• Gastrointestinal disease is a major contributor to adult mortality in captivity. Potential causes include husbandry factors (cold, stress, parasitism)

Squirrel monkeys

Evidence of harm associated with captivity.

• A preference for high energy food puts squirrel monkeys at risk of obesity.
• Living in isolation is associated with a greater risk of stereotypies.

More information is needed to understand the welfare of this animal.

• The natural behaviour of squirrel monkeys (and primates in general) is altered by hand-rearing and the consequences of this for stress-coping are unknown.

Key resources (primates)

EAZA Best Practice Guidelines for Callitrichidae (Ruivo and Stevenson, 2017)

Code of practice for the welfare of privately-kept non-human primates (Defra, 2010)

Nonhuman Primate Dental Care. (Johnson-Delaney, 2008)

“Do you give a monkey’s” The need for a ban on pet primates (RSPCA, 2016).

The welfare of primates as pets in England: call for evidence Summary of responses and way forward (DEFRA, 2020)

EAZA best practice guidelines: Capuchin Monkeys (Souvignet et al., 2019).

AZA Eulemur care manual (Campbell et al., 2013).

1.5. Marsupials

Sugar gliders (Petaurus breviceps) and Bennett’s wallabies (Notamacropus rufogriseus; formerly Macropus rufogriseus) are two of the most common pet marsupials encountered by veterinary surgeons in the USA (Brust, 2009). Wallabies are herbivorous foregut fermenters with a chambered stomach (Munn, Banks and Hume, 2006). Sugar gliders have a large caecum, which is the site of gum fermentation (Brust, 2009).

1.5.1. Sugar gliders

A Web of Science search yielded only 11 search results relevant to keeping sugar gliders as pets.

a) Breeding

No information was found on the conditions of sugar gliders in breeding facilities. Two articles were published on the topic of surgical castration (scrotal ablation) (Cusack et al., 2017; Malbrue et al., 2018). Both techniques, using a “LigaSure” device (Cusack et al., 2017), and electrosurgery (Malbrue et al., 2018), were found to be safe and effective in the small cohorts tested (five and eight males respectively).

b) Housing requirements

The RSPCA “Handle with Care” report (RSPCA, 2004) identifies aspects of the natural behaviour of sugar gliders that pose particular difficulties for private ownership of sugar gliders in captivity. Sugar gliders are social and nocturnal (zoo sugar gliders (Dierenfeld and Whitehouse-Tedd, 2018) slept from 6am to between 7-9pm). A challenge to the captive housing of sugar gliders is their arboreal nature. As the name suggests, their behavioural repertoire involves gliding. The 2004 “Handle with Care” report highlights the fact that sugar gliders rarely come down to the ground from tree canopies, and “can glide for as far as 45 metres between trees”. Heat should be provided at 21-32 ^oC, so that the provision of an adequate tree canopy, along with an appropriate climate to encourage levels of activity observed in the wild, is extremely challenging.

Guidance on the care of sugar gliders was published in “Seminars in Avian and Exotic Pet Medicine” (Booth, 2003), most of which is based on the experience of a specialist veterinarian working with Australian native species and knowledge of their natural history, rather than published studies of captive animals. The author recommends that housing less than 2m x 2m x 2m is inappropriate, which should include a nest box, vertical and horizontal branches, raised feeding stations and sleeping quarters. Housing of sugar gliders is described as commonly “in small bird cages, with a suspended pouch provided as sleeping quarters”, which the author states may be appropriate as long as supervised exercise is given regularly outside the cage.

c) Nutrition

Sugar gliders are described as facultative gummivores; they are adapted to a low-moderate protein diet and obtain calcium and other minerals from gums. They mainly eat insects, spiders and plant exudates in the autumn and winter (Brust, 2009). Their main energy source is from non-foliage plants, including saps, manna, necor, resins, honeydew, lerp and plant gels (Dierenfeld et al., 2006), and this natural diet is difficult to replicate in captivity (Dierenfeld and Whitehouse-Tedd, 2018). Disorders related to inappropriate diet may include obesity, osteodystrophy, malnutrition and dental disease (Ness and Booth, 2004). This review did not find any information on the incidence of these diseases in the pet population. Hypocalcaemia results in fractures, paresis, paralysis and ataxia (Brust, 2009).

Feeding trials were carried out on nine male sugar gliders (4-9 months old) over the course of two months with three animals per treatment. The findings demonstrated that sugar gliders selectively eat preferred ingredients from mixed diets, consuming most (75-100%) of the high energy foods: meat (chicken and meal worms) and fruit mixes, and consuming least of the vegetable component (38-51%). Variation within trial groups was high (two gliders in group C lost weight and the third had the greatest weight gain overall). Therefore, it is not possible to conclude which diet was most likely to result in obesity. Health and mineral status were measured, but sample size restricted the conclusions that could be drawn about the impact of each diet.

A larger trial was carried out of three diets fed to 12 gliders using a cross-over design, so that all animals experienced all diets. The diets are described in detail (Dierenfield and Whitehouse-Tedd, 2018) and briefly summarised in Box 1.

Box 1: Three diets for sugar gliders, analysed by (Dierenfield and White-house Tedd, 2018)

Diet 1: Liquid formula and a mix of fruit and vegetables.

Formula (from powder): Dried honey, dried egg product, dried whey protein concentrate, bee pollen, soya protein concentrate, vegetable oil, cereal grains, and vitamin and mineral premixes.

Produce mix: Peas, green beans, carrots, lima beans, green peppers, cucumber, papayas, strawberries, raspberries, blackberries, bok choy.

Diet 2: Home-cooked ingredients plus protein and calcium supplements

Orange juice, honey, water, two cooked eggs, chicken or turkey jarred baby food, yoghurt, bee pollen

Produce mix (as for diet 1).

Protein Supplement: Whey protein, soya protein, processed cereals, maltodextrin, dextrose, mannan oligosaccharides, β-glucans, lysine, methionine, vegetable oils, omega-3 and -6 fatty acids, carotenoids, taurine, vitamins and minerals.

Calcium carbonate powder

Diet 3: Pellets and gravy

Pellets: Ground whole cereal grains, soya meal, flax meal, corn gluten meal, whole dried eggs, dried whey, fish meal, minerals, vitamins, microbial enzymes and probiotics.

Gravy: Dried honey, dried egg product, dried whey protein concentrate, bee pollen, soya protein concentrate, vegetable oil, cereal grains, vitamins and minerals, water.

Diet 2 caused weight gain and diet 3 caused weight loss, whereas weight did not change significantly during the feeding of diet 1. Weight gain on diet 2 was associated with a greater dry matter intake (per body weight) and caloric intake, compared with diets 1 and 3. Across all diets, protein digestibility was similar to natural diets. The authors advise that the protein level of these diets is still likely to be higher than necessary for good health. Mineral digestibility varied for magnesium and phosphorus (higher in diets 1 and 2 than diet 3), and iron and zinc digestibility was higher in diet 2 than diet 3. Only diet 3 provided appropriate Ca and P concentrations and ratios, whereas Diet 1 and Diet 2 were both low in Ca relative to P, and high in K, likely due to the fruit content. Notably, none of the diets contained gum. The authors conclude that these diets are likely to support good health and, compared with insect feeding, the constituents are more reliable in nutritional value. Commercially formulated ingredients seemed to provide more appropriate Ca: P ratio than the more home-cooked rations (diets 1 and 2).

1.5.2. Wallabies

Few studies were found on Web of Science.

a) Transport and handling

Wallabies are vigilant towards zoo visitors and it may be that humans are perceived as predators (Meade et al., 2021).

b) Health and disease

In the USA pet wallaby population the most common infectious gastrointestinal disorders are macropod progressive periodontal disease (MPPD, or “lumpy jaw”), candidiasis, toxoplasmosis, campylobacteriosis and Tyzzer’s disease. Parasites are often diagnosed but seem to not cause clinical disease (Brust, 2009).

MPPD is a serious, often fatal disease in captive wallabies, with a prevalence in European zoos of 4.9 cases/100 animal years and in Australia of 5.7 cases/100 animal years (Rendle et al., 2020). Bacterial infection is involved, in particular Fusobacterium necrophorum. Feeding and husbandry affects the likelihood of MPPD, and cold climates are cited as a risk factor (Oliphant et al., 1984), but Rendle et al., (2020) found that the prevalence of cases in Australian and European zoos was not affected by geographical region. There is a link between relocation to a different enclosure or between zoos and MPPD. Therefore, transport or relocation stress is a possible risk factor (Rendle et al., 2020). This review did not include any studies which included behavioural or physiological parameters of stress around relocation in wallabies, but a link between stress and MPPD has been shown in kangaroos (Sotohira et al., 2017). A risk factor for the entry of bacteria is the feeding of “spiky” food, or the occurrence of periodontal disease, which is common in wallabies (associated with feeding large amounts of soft, sticky food) (Brust, 2009).

Summary: Marsupials

Biological or behavioural needs which are difficult to provide in captivity.

• The dental health of captive marsupials is a concerning issue and the feeding of an appropriate diet is difficult due to their seasonal variation in feeding behaviour in the wild, including facultative or obligatory consumption of plant exudates.
• The environmental and behavioural needs of sugar gliders are not compatible with living in small spaces; adequate cage sizes must be combined with being taken out regularly for exercise.

Key resources

“Handle with care” report (RSPCA, 2004)

Sugar Gliders (Booth, 2003)

Evaluation of three popular diets fed to pet sugar gliders (Petaurus breviceps): Intake, digestion and nutrient balance. (Dierenfeld and Whitehouse-Tedd, 2018)

2.0. Birds

The birds covered in this review are: Parrots (African grey parrots, Amazon parrots cockatoos, eclectus parrots, macaws and ring-necked parakeets), finches (except for canaries), and birds of prey (barn owls, eagles, eagle owls, Harris’ hawks, and lanner, saker and peregrine falcons).

The Pet Food Manufacturers’ Association estimates there are 30,000 indoor pet birds in Scotland (from 2019 using average figures over three years) (Pet Food Manufacturers’ Association (PFMA), 2021), with an average of 1.6 birds in 20,000 bird-owning households. Therefore, although the distribution of birds per household is not stated, it is very likely that the social needs of birds are not being met in captivity. Parrots have long lifespans and the Oasis Sanctuary (USA) has requests for help in rehoming 1000 to 1500 parrots per year, partly because the birds can outlive their owners, who purchase pets in retirement (“the need for rescue and sanctuary in the 21^st century), but also because owners find their birds “too destructive, time consuming, loud or expensive”, because of changes in relationships, new babies and new jobs (Oasis Sanctuary Foundation Ltd., 1997-2006).

Birds are not included on “positive lists” in Europe, except in Croatia, Luxembourg and Malta. A scoring system was developed to inform beginner or unqualified pet keepers of exotic animals about how difficult they are to keep (Easy, Moderate, Difficult or Extreme, or “Emode”) and scores have been calculated for some of the species in this review (Warwick et al., 2018) (Table 2), which indicate the majority are very challenging pets. In comparison, rats (Rattus norvegicus) were assigned a score of 10 points and fall into the category “easy to moderate”. The parrots in this review are listed in CITES Annex A and therefore all captive bred birds require closed leg-rings with unique identifying numbers. Pets do not need to be registered, but any commercial activity must be certified by DEFRA.

Table 2. Selected “ EMODE” scores calculated on the website www.emodepetscore.com, describing the level of difficulty required to keep birds as pets.

Type of bird	Points (+ 5 points if a household member is vulnerable)	Category
African grey parrot, Psittacus erithacus	33	Extreme
Amazon parrot, Amazona spp.	33	Extreme
Umbrella cockatoo, Cacatua alba	38	Extreme
Blue-and-yellow macaw, Ara ararauna	33	Extreme
Hyacinth macaw, Anodorhynchus hyacinthinus	33	Extreme
Gouldian finch, Chloebia gouldiae	23	Difficult
Zebra finch, Taeniopygia guttata	18	Moderate to difficult
Harris’ hawk, Parabuteo unicinctus	23	Difficult

There are fundamental questions about the keeping of birds in captivity. The act of placing a bird in a cage may be sufficient to cause stress, unless the enclosure is so large and well equipped that the bird does not perceive it as captivity (Graham, 1998). The ideal enclosure may exceed the means of the average private owner. Flight and socialisation are particularly challenging natural behaviours to accommodate in captivity (Engebretson, 2006).

2.1. Parrots

Statements from the Parrot Welfare Trust (in the interim report) identified some key areas of concern, where owners’ lack of understanding or failure in provision result in suffering. These can be summarised as: Nutritional deficiencies (especially vitamin A and calcium), unbalanced diets (macro- and micronutrients), over-feeding, failure to provide UVB lighting and air purification, and failures in biosecurity. Causes of psychological suffering include inadequate cage sizes and wing clipping. The list of illnesses linked to poor husbandry is extensive: Respiratory infections, fungal infections, seizures, weakness, difficulty laying eggs, liver disease, muscle wastage/inability to fly, obesity, chlamydiosis, Psittacine Beak and Feather Disease (PBFD), avian bornavirus and food toxicities. The Parrot Society provides care sheets and publishes a magazine, both of which are only available to members (www.theparrotsocietyuk.org).

A review of environmental enrichment for parrots (Rodriguez-Lopez, 2016) found that most studies evaluate enrichment in terms of its effects on activity budget (e.g., increasing activity or stimulating foraging) or reducing abnormal behaviours. Foraging activity is markedly reduced in captivity. Wild parrots spend around 40%–75% of their waking time searching for or accessing food, compared with 42 mins. in captive orange-winged Amazon parrots, Amazona amazonica (Rozek and Millam, 2011). Beyond these functions, enrichment should allow parrots control over their environment, and to fulfil their social needs, e.g., social play (Diamond and Bond, 2003). Studies carried out in a laboratory setting (Mettke-Hofmann, 2000; Garner et al., 2003; Meehan et al., 2003; Fox and Millam, 2004; Meehan et al., 2004; Lumeij and Hommers, 2008; Kim et al., 2009; Rozek et al., 2010; Webb et al., 2010; Rozek and Millam, 2011; van Zeeland et al., 2013; Cussen and Mench, 2015) may be more applicable to pet parrots than enrichment studies in zoos, since social deprivation, exposure to human handling and space restrictions are very relevant to both the laboratory and the home. Meehan and Mench (2002) carried out regular handling of their Amazon parrots, so they would be suitable to rehome as pets after the experiment.

2.1.1. African grey parrots, Psittacus erithacus

a) Behaviour

Feather destructive behaviour is an abnormal repetitive behaviour, which constitutes a major welfare problem, frequently observed in pet African grey parrots, Psittacus erithacus (Greenwell and Montrose, 2017). This problem has been attributed to a lack of adequate resources to develop coping skills. An active/ bold personality type may predispose individuals to developing FDB (van Zeeland et al., 2013). Secondary to self-mutilation, opportunistic bacterial infection can be serious and chronic. Positive resolution can be achieved in almost all cases with appropriate care, but can take up to 21 months to achieve (Abou-Zahr et al., 2018).

Aggression was observed in both parrots that bonded to a human and those that did not, and mostly in birds between four and seven years of age. Inappropriate hand-rearing practices (such as feeding chicks with tubes) or early painful experiences can lead to a fear of humans, which leads to biting (Welle and Luescher, 2008), and territorial aggression is also seen (Gaskins and Bergman, 2011). A large survey (103 pet P. erithacus over three years of age of known origin) explored the risk factors associated with different types of hand-rearing, parent-rearing and wild-capture. Hand-rearing was associated with greater aggression, whereas wild-caught birds had poorer health and more abnormal behaviour. Captive parent-rearing appears to be a balanced approach between the extremes of hand-rearing and wild capture, but the time at which birds are separated from their parents is critical, and parent-rearing was associated with a greater risk of the juvenile behaviour of demanding food directed at owners extending into adulthood (Schmid et al., 2006). Owner behaviour (aggression or shouting towards the bird, often in response to unwanted behaviours) can exacerbate aggression.

A lack of social and cognitive stimulation is an issue in pet African grey parrots, and FDB may arise as a consequence of frustration and suffering caused by a lack of appropriate company and stimulation. Owners should not acquire an African grey parrot, if they cannot spend a minimum of four hours per day with the pet; the risk of feather picking decreased by nearly 90% when birds interacted with humans for more than four hours per day (Gaskins and Hungerford, 2014). Pair-bonding can be challenging, if a new parrot is introduced to an established pair. However, social isolation, as associated with shorter telomeres (Aydinonat et al., 2014), indicates these birds are suffering chronic stress.

b) Housing requirements

In common with other parrots foraging is a major part of their natural behavioural repertoire and can be stimulated using feeding enrichments. Eleven types of foraging enrichment were compared (van Zeeland et al., 2013) and the longest foraging duration was around two hours per day, which was achieved with a “Plastic foraging device consisting of four opaque cups that can be hung from the ceiling and need to be unscrewed” and a “Honey-comb transparent acrylic feeder (W × L = 8 × 18 cm), in which a cardboard box filled with food can be placed”.

2.1.2. Amazon parrot

EAZA has produced best practice guidelines for the Ecuadorian Amazon parrot, Amazona lilacina (Pilgrim and Biddle, 2016), but it is unlikely that enclosure design, rearing and handling advice is going to be applicable to owners of Amazon parrots, unless they have the space and means to provide zoo-like conditions. The guidelines highlight the importance of disease screening, which is relevant to parrot importers and breeders of all species.

a) Behaviour

The University of California, Davis has a research centre for Parrot Wellness and Welfare. A colony of orange-winged Amazon parrots has been the focus of a number of studies on enrichment (Meehan et al., 2003; Meehan et al., 2004; Kim et al., 2009; Rozek et al., 2010; Webb et al., 2010). This work elucidates the link between social isolation, lack of environmental complexity and foraging opportunities on poor psychological wellbeing and the incidence of stereotypical behaviour. Early experience in chicks, but not necessarily rearing method, has an important influence on the neophobia of adult parrots (Fox and Millam, 2004).

b) Nutrition

Complete pelleted diets are readily available for pet parrots in the UK, which are formulated to provide appropriate energy requirements as well as adequate levels of vitamin A and calcium: phosphorus ratios (Brightsmith, 2012). However, pellets can be perceived as monotonous, may be unappealing and feeding a high-seed diet is preferred by some owners, which can result in selective feeding and nutrient imbalances. A small study (seven adult parrots, fed a mixed diet with a higher proportion of seeds (25%), consumed less calcium, sodium and iron, and more than the recommended amount of fat. At lower levels of seed feeding (18%), fat consumption was still above recommended levels. Amazons, which were given mostly pellets (75%) with 25% fresh produce, consumed a recommended balance of nutrients. In recent nutrition studies for Amazon parrots, palatability of processed foods was tested, which should improve uptake (Di Santo et al., 2019; Werneck et al., 2020).

c) Health and disease

Atherosclerosis is a common disease of both African grey and Amazon parrots, and a common cause of sudden death among parrots submitted for necropsy (Fricke et al., 2009). This literature search did not find any more recent estimates of the incidence of these diseases, since Bavelaar and Beynen analysed the causes of atherosclerosis in parrots (Bavelaar and Beynen, 2004). As in humans, atherosclerosis is linked to plasma cholesterol and has genetic, dietary and lifestyle-related causes. Abnormalities in heart dimensions are associated with obesity in blue-fronted Amazon parrots, Amazona aestiva (dos Santos et al., 2020).

2.1.3. Cockatoos, Family Cacatuidae

a) Behaviour

Behavioural issues were the most common results of the Web of Science search, including a study of visitor behaviour in zoos (Collins and Marples, 2015). Citron-crested cockatoos, Cacatua sulphurea citrinocristata, became more social in the presence of visitors, when housed near a zoo playground. Facial expression of positive welfare is associated with feather ruffling over the cheeks and nape (Bertin et al., 2020).

Cockatoos, in common with other parrot species, express abnormal repetitive behaviours in response to the captive environment. Simple materials that are easily accessible in the UK, but which can significantly decrease stereotypical behaviour, are fresh grass and millet discs (Fangmeier et al., 2020). Cockatoos, along with African grey parrots, are at most risk among parrots for feather-destructive behaviour, according to a multi-country survey of 42 cases and 126 controls (Gaskins and Hungerford, 2014). This finding was replicated in UK populations; a survey of 310 cockatoos found that 42.4% of cockatoos had expressed feather-destructive behaviour at some point during their life (Jayson, Williams and Wood, 2014). Most (62.9%) plucked more than one body area. Being acquired from a pet shop had a considerable influence on feather-plucking, with cockatoos from pet shops having a six-fold greater risk than those bought from private breeders. Keeping the cage against a wall increased the risk of feather plucking. Being male, having owners that were away for more than one week, being regularly sprayed with water and command training were also risk factors. For both cockatoos and African grey parrots, 50 potential causes were tested and most were found to be insignificant influences on the incidence of feather-pecking. Veterinary treatment may be required for the treatment of feather damage caused by owner feather trimming (Welle, 2019).

b) Mortality

In Canada over a period of 19 years, when causes of mortality in more than 20 different genera of captive psittacine birds were analysed (Gibson et al., 2019), cockatoos were not significantly more affected by any of the categories of disease than any other parrot genus. Non-infectious, metabolic causes of death were most common, such as atherosclerosis, gout and haemosiderosis. Haemorrhage, congestion, degenerative diseases (such as atrophy and necrosis) were commonly diagnosed. The most common infectious causes of death included bornavirus, polyomavirus, circovirus, Mycobacterium spp., Chlamydia spp., Macrorhabdus ornithogaster and Aspergillus spp .

2.1.4. Eclectus parrot, Eclectus roratus

Of 16 search results on Web of Science using the terms defined in this review, 13 were health-related, two were related to breeding in wild eclectus parrots (Heinsohn et al., 1997; Heinsohn and Legge, 2003) and one studied the nutritional intake of nestling eclectus chicks in Indonesia (Rachmatika et al., 2020).

a) Behaviour

Eclectus parrots feature in studies of feather-plucking (Garner et al., 2008; Horie et al., 2012; Grosset et al., 2014), a condition which is discussed in general terms in section 2.0.

b) Health and disease

The literature was sparse and dominated by case reports of diagnosed conditions in a single parrot (disseminated coelomic xanthogranulomatosis, (Donovan et al., 2022); intracoelomic teratoma, (Mayer et al., 2021); mycobacteriosis, (McRee et al., 2017); osteoma, (Cowan et al., 2011); complications after orthopaedic surgery (Harris et al., 2007); immune-mediated haemolytic anaemia (Johnston et al., 2007); and ventricular diverticulum (De Voe et al., 2003). Eclectus parrots are amongst those most affected by Psittacine Beak and Feather Disease in Taiwan (Lin et al., 2021). They can also host microfilaria parasites (Huang et al., 2017), although this study was also from Taiwan and there is no evidence to suggest microfilaria is a problem in UK parrots.

2.1.5. Macaws

a) Breeding

Formulas available for hand-rearing parrots do not match the crop contents of wild chicks. Although they have comparable energy content, they may be lacking in minerals and electrolytes, including potassium, magnesium and manganese (Cornejo et al., 2013). Overall, formulas for hand-rearing vary between brands and although research is continuing, e.g., the characterisation of fatty-acid profiles appropriate for feeding young chicks (Cornejo et al., 2021), more work is needed to ensure such diets are standardised and provide the appropriate balance of nutrients (but see Schmid (2006) for evidence on the outcomes of hand-rearing parrots).

b) Behaviour

Macaws share characteristics with other psittacine birds, including the expression of stereotypical behaviours (de Almeida et al.,2018), in the captive environment, which are exacerbated by lack of appropriate enrichment. Physical, feeding and cognitive enrichments all stimulate activity (Miglioli and Vasconcellos, 2021), although no significant relationships were found in this study between enrichment and reproductive success. Among parrots, macaws are particularly large and easily capable of injuring their owners.

c) Nutrition

Veterinary investigations have defined physiological values of vitamins A and E in psittacines, including macaws (Torregrossa et al., 2005); haematology and biochemistry values for hyacinth macaws, Anodorhynchus hyacinthinus (Kolesnikovas et al., 2012); haematological values of green-and-red macaws, Ara chloropterus (Vieira et al., 2021).

2.1.6. Ring-necked parakeet

Ring-necked parakeets, Psittacula krameri, are the only parrot species successfully free-living in the UK. The only WoS results from the pre-defined search terms related to free-living parakeets in the UK (Newson et al., 2011; Sa et al., 2014; Heald et al., 2020), France (Pisanu et al., 2018) and Portugal (Rocha et al., 2020). Avihepadnavirus has been identified as a cause of liver disease in young birds in Poland (Piasecki et al., 2013). Chlamydia psittaci, isolated from swabs of multiple organs in psittacine birds, including suburban populations of ring-necked parakeets in France (Pisanu et al., 2018), is an important cause of disease and of particular concern as a zoonosis (Gibson et al., 2019).

Summary: Parrots

Biological or behavioural needs which are difficult to provide in captivity.

• The dietary needs of parrots require not only nutritional, but behavioural understanding of the species, which may require a concerted effort to overcome selective feeding.

Evidence of harm associated with captivity.

• Aggressive or reactive biting can escalate negative interactions between parrots and their owners and become a barrier to giving parrots the appropriate amount of positive, active time out of their cages.
• Parrots’ behavioural responses to a lack of appropriate social and mental stimulation are very dramatic and can result in intractable, distressing feather-damaging behaviour.
• Atherosclerosis can cause severe cardiac disease, including sudden death, and although dietary factors play an important point in mitigating this, parrot breeders should also avoid selecting for individuals predisposed to this condition.

More information is needed to understand the welfare of this animal.

• The effect of relinquishment and rehoming on parrots should be investigated, as these are long-lived, demanding pets, vulnerable to the consequences of becoming unwanted pets.

Key resources

EAZA Best Practice Guidelines, Ecuadorian Amazon Parrot (Pilgrim and Biddle, 2016)

Prevalence and risk factors of feather plucking in African grey parrots (Psittacus erithacus erithacus and Psittacus erithacus timneh) and cockatoos (Cacatua spp.). (Jayson et al., 2014)

The gray matter: Prevention and reduction o).f abnormal behavior in companion gray parrots (Psittacus erithacus) (Greenwell and Montrose, 2017.)

The welfare and suitability of parrots as companion animals: A review. (Engelbretson, 2006).

The Parrot Society www.theparrotsocietyuk.org

2.2. Finches

The most commonly kept species of pet finch in the UK is the zebra finch, Taeniopygia guttata. These are also common laboratory animals, e.g., in studies of song learning, flight, navigation and foraging (Patterson and Fee, 2015). The Association for Avian Veterinarians provides a basic care guide for “companion birds” (AAV, 2019), which, for finches, has few specific recommendations, but highlights the need for spaced-apart perches to allow hopping and flying, the benefit of keeping finches socially and encourages owners to provide long, large enclosures for flight, and social companions. Wild capture of finches in the UK is illegal, but according to the RSPB is still common (RSPB, n.d.).

a) Behaviour

Finches form pair-bonds and are prolific breeders (RSPCA, 2011). Fear is also a concern, if birds are not used to humans. The effect of isolation on finches (other than canaries) is not published, but canaries, Serinus canaria, have a more positive cognitive bias, if housed socially rather than alone (Lalot et al., 2017). Zebra finches score 18 EMODE points (23 if a family member is vulnerable), whereas Gouldian finches (Chloebia gouldiae) score higher (23 points) due to being “an especially sensitive species”.

b) Housing requirements

The RSPCA provides a guide to housing and care of zebra finches (RSPCA, 2011). This guide provides references, including “The Zebra Finch: A synthesis of field and laboratory studies” (Zann and Bamford, 1996). Popular pet songbirds, such as zebra finches and Gouldian finches, are adapted to the climate of Australia, but no published studies were found on the effect of a colder climate on their welfare. Acute, loud noises cause short-term disruption of birds’ behaviour (at least 15 minutes after a fire alarm, (Corbani et al., 2021). Bathing water is an important resource for zebra finches, as demonstrated by (Krause and Ruploh, 2016). Without the opportunity to bathe for 30 days, finches had a higher basal cortisol plasma concentration.

c) Nutrition

Finches’ natural diets vary seasonally and they require grit to aid digestion (Patterson and Fee, 2015). Publications on nutrition are often in the context of development (from an ecological research angle, in relation to song learning (Lovell et al., 2011; Yamada and Soma, 2016) or reproduction (Blount et al., 2003; Blount and Matheson, 2006; Noguera et al., 2017), rather than demonstrating a relationship with good health or clinical disease.

Summary: Finches

Biological or behavioural needs which are difficult to provide in captivity.

• Owing to their popularity and use in research, information is available on appropriate aviary design and social needs, which can allow finches to perform normal behaviours.
• Finches can habituate to human presence, but require company of their own kind.
• Finches form stable breeding pairs therefore allowing this normal social behaviour is difficult as uncontrolled breeding is usually not compatible with pet ownership.

More information is needed to understand the welfare of this animal.

• Evidence of the welfare of finches kept in domestic situations other than aviaries is lacking. Finches kept in small cages which do not allow for flight, or kept in social isolation are at risk of poor welfare, but this has not been investigated.

Key resources

Basic care guide for companion birds (Association for Avian Veterinarians, 2019).

Zebra finches: good practice for housing and care (RSPCA, 2011).

2.3. Birds of prey

This review did not elicit evidence about the welfare of birds of prey in private ownership in Scotland. EAZA publish guidance on falconry demonstrations (Habben and Parry-Jones, 2016) , including aviaries, transport, tethering, training, free flight and breeding. This evidence is a result of a collaboration between zoo experts and representatives of the Hawk Conservation Trust.

2.3.1. Barn Owl, Tyto alba

The Barn Owl Trust (Barn Owl Trust, 2021) does not recommend keeping barn owls as pets, nor for falconry birds. They state many reasons why barn owls do not make good pets: Stroking their feathers reduces natural waterproofing, they are not suitable to be kept indoors, mostly inactive unless hungry, can show persistent juvenile calling for food or aggression if imprinted to a human “parent” and during the breeding season, and males can be very noisy at night. Untamed barn owls prefer to be away from people and stay out of sight. Owls are not easy to train with food, and they are nocturnal and once they are fed, prefer to rest and digest their food. Flying off while wearing ankle straps can cause the bird to become trapped and die. Additional considerations include unwanted breeding, difficulty in finding holiday care and the relevant legislation for keeping the species: It is illegal and unethical to release a captive barn owl. Reference values are established for haematology and blood biochemistry parameters in healthy barn owls (Szabo et al., 2014; Agusti Montolio et al., 2017, 2018).

2.3.2. Eagles, Family Accipitridae and 2.3.3. Eagle owls, Bubo spp.

There were few studies relevant to the welfare of captive eagles or eagle owls in the Web of Science search. A retrospective study of pododermatitis (bumblefoot) in rehabilitated raptors in the USA reported an incidence of 52 cases per 100 bird-years at risk between 1980- 1990 and this disease was described as being “one of the most common and potentially serious afflictions of captive raptors” in the proceedings of an American veterinary conference held in 2001 (Forbes, 2001). A lower prevalence has been reported from Spain, data on 2004 raptors admitted to a wildlife rehabilitation centre (Madrid) included 8.8 cases/ 100 bird-years at risk. Accipitridae were more at risk than raptors from the Falconidae and Stringdae families. No studies reported on the prevalence of infectious diseases among captive eagles in the UK, but a study of adenoviral disease outbreaks in a UK bird “collection” identified a previously unknown virus, “raptor adenovirus”, which was causing deaths, including of two owls (Zsivanovits et al., 2006). Successful surgical treatment of a calcified lesion in a captive-bred tawny eagle, Aquila rapax (calcinosis circumscripta) was described (Sabater et al., 2016). Another case report by the same author reports that intussusception, an emergency intestinal obstruction requiring surgery, is rarely reported in raptors (Jones et al., 2004). A golden eagle, Aquila chrysaetos, presented with acute trauma during exercise, leading to spinal fracture and spinal cord compression, and was subsequently euthanased (Fraga-Manteiga et al., 2013).

2.3.4. Harris’ hawks, Parabuteo unicinctus

Feather-destructive behaviour is reported in Harris’ hawks more commonly than in other captive raptors (Smith and Forbes, 2009). An article published in the USA (Jones, 2004), describes behavioural aspects of captive birds of prey. Harris’ hawks, used for falconry, can pose a risk to immune-compromised humans (see appendix 1). Evidence for the welfare of captive Harris’ Hawks in the scientific literature is lacking.

a) Breeding

The early period when the young bird is in the nest involves imprinting, when it learns to recognise parents and siblings, and then later learning about future mates. A long period of daily socialisation is required in order for raptors to imprint (i.e., accept) a human as a surrogate parent or mate. The sensitive period varies according to species and nocturnal birds imprint later in development than diurnal birds. Food-begging, screaming and aggression are described as commonly occurring behaviours, which make raptors challenging in captivity. No recent reviews or case reports of behavioural issues were found (Jones, 2004).

b) Housing requirements

The British Falconers’ Club recommends that a Harris’ hawk is the most appropriate bird to begin training for a novice falconer, but that they do not make good pets, and ownership should follow careful consideration and study. Owning a hawk involves dedication of considerable time, accommodation, daily feeding of raw food, training, and crucially, the continuous assistance of an experienced falconer.

c) Health and disease

Atherosclerosis, which can lead to hypertrophy of the left ventricle, and in the most extreme cases, sudden death by myocardial infarction (Legler et al., 2017), is reported in Falconiformes (diurnal birds of prey) and Strigiformes (owls) (Jones, 2013), but the prevalence of this disease in UK populations has not been recently reported (Mitchinson and Keymer, 1972). The risk factors for this disease are thought to be associated with captive diets, obesity and lack of exercise (Jones, 2013). Similarities between this condition in humans, raptors and owls, include an increased risk associated with elevated blood cholesterol. Birds fed a diet of day-old chicks rather than rats and mice were at a higher risk of having increased serum cholesterol (Legler et al., 2017).

2.3.5. Falcons, Falconidae

a) Transport and handling

Lanner, Falco biarmicus, and saker falcons, Falco cherrug, at a rehabilitation centre in Jordan were most commonly presented due to illegal ownership and confiscation at the port of entry (five of seven lanner falcons, six of 10 Saker falcons). Three lanner falcons had coccidiosis; other reasons for rehabilitation were sporadic incidences of trauma or disease (Al Zoubi et al., 2020).

The effect of transport on blood-cell values was tested in peregrine falcons, Falco peregrinus, and Harris’ hawks, Parabuteo unicinctus (Parga et al., 2001). Peregrine falcons, which were accustomed to transport, did not show any significant changes in blood-cell parameters after one hour of transport, and for those which were untrained, their heterophil/ lymphocyte ratio increased (suggesting this was more stressful for the untrained birds). Among Harris’ hawks, more blood changes were observed; the untrained birds showed leucopaenia, lymphopaenia and eosinopaenia, whereas trained birds had monocytosis.

b) Health and disease

Outside the UAE (United Arab Emirates) (Lierz et al., 2002) and Kuwait (Tarello, 2008), no studies on the health or welfare of saker falcons were found since 2001. In the Czech Republic, one hybrid saker falcon x gyrfalcon (Falco cherrug x F. rusticolus) and one Harris’ hawk died during an outbreak of West Nile virus encephalitis (Hubálek et al., 2019). Falcons can become ill due to aspergillosis, which is often secondary to immune suppression or concurrent bacterial infection. A review of appropriate treatment regimes was carried out (Krautwald-Junghanns et al., 2015). Supportive therapy alongside antimycotic drugs is necessary in most cases. Protozoal diseases, Caryospora spp., also affect falcons and owls.

Summary: Birds of prey

Biological or behavioural needs which are difficult to provide in captivity.

• Taming birds of prey to make them amenable to living around humans, by handling them as chicks, is not always successful and can result in adults, which are unsuitable for release and have poorer welfare in captivity.
• Free flight gives birds of prey the exercise and expression of normal behaviours they need, and evidence for the provision or absence of this opportunity in the pet population is unknown.

Evidence of harm associated with captivity.

• Based on the information provided by hobbyist organisations, there are significant risks to bird welfare, if ownership is entered into without the appropriate expertise and guidance, and some species are not suitable as pets.

More information is needed to understand the welfare of this animal.

• There was no evidence on the welfare of birds of prey kept as pets in Scotland.

Key resources

EAZA Falconiformes and Strigiformes Taxon Advisory Group Husbandry and Management Guidelines For Demonstration Birds (Habben and Parry-Jones, 2016).

3.0. Fishes

The fishes covered in this review are cichlids, Order Cichliformes, clownfishes, Subfamily Amphiprioninae, Koi carp, Cyprinus rubrofuscus, and Siamese fighting fish, Betta splendens. The welfare issues of fishes on their journey to the home aquarium are not often measured at the species level and some general issues are outlined here.

a) Transport and handling

The scale and sustainability of the ornamental pet trade is outside of the scope of this review, but is explained in a recent publication (King, 2019). Captive-breeding of marine oriental fishes is mainly carried out in non-EU countries, such as Indonesia, the Philippines, USA and Sri Lanka. Imported fishes from third (non-EU) countries into the UK are accompanied by a packing list, which details the species and their quantities, but this information is not available in a repository (King, 2019). Overall rejection rates of wild-caught marine aquatic fishes are suggested by King (2019) to be lower than the 24.2% in a six-month period figure stated in a small study from Papua New Guinea (Militz et al., 2016), with the rationale that countries with more established industries have more experienced operators and divers paid by the number of fish they catch that are subsequently exported, but more quantitative data are needed to confirm this. A recent estimate of the number of marine ornamental fishes imported into the UK between 2012 and 2014 is 1.4 million (Defra, 2015).

The average transport time for ornamental fishes sold in the UK is 24 hours (Vanderzwalmen et al., 2021). Therefore, welfare in transport is a pressing issue relevant to all ornamental marine fishes. Ornamental fishes are subject not only to deterioration in water quality, because of the build-up of waste products of the fishes being transported, but to abrupt changes in water at different stages of the supply chain (Vanderzwalmen et al., 2021). In addition to issues of water quality and temperature, handling is a profound stressor (Portz et al., 2006), and in cichlids, packing into plastic bags, is associated with a four-fold rise in cortisol in the subsequent two hours, which continued to increase until six hours post-packing (Wu et al., 2021). Sedatives and tranquilisers are used routinely (Crosby et al., 2010), but doses used may not be standardised, evidence based and safe. Dried soybean root (Glycine tomentella) was demonstrated to reduce cortisol at four hours post simulated transport in orange-spotted grouper, Epinephelus coioides, blood parrot cichlids, Amphilophus citrinellus x Vieja melanurus, and koi carp (Wu et al., 2020, 2021).

(Baldisserotto et al., 2014) studied the effect of transport on cardinal tetras (Paracheirodon axelrodi) under normal commercial conditions for a 24-hour journey between Barcelos and Manaus, Brazil. Mean survival was 99.5%, with no significant effect of treatment with salt water, tetracyclines or Amquel^®, which are commonly used in the transport of commercial fishes to reduce transport stress. Whole body cortisol increased during the initial three hours and this increase was mitigated by the addition of any/all additives (however, the massive increase in Na+ and Cl- influxes, and the potential to develop antibiotic-resistant pathogens suggest these additives should not be used routinely). After this time cortisol decreased back towards baseline by 24 hours after treatment, suggesting that the processes associated with catching, loading, change in water and/or changes in the social environment have a greater effect on the level of stress experienced by fish compared with the journey duration and associated water quality issues. Transport in sealed plastic bags leads to the accumulation of CO₂ and consequent drop in pH, whereas fish in open containers are subject to a slower decrease in pH and are less stressed.

DEFRA do not provide specific guidance for the welfare of fish during transportation (www.gov.uk/guidance/animalwelfare#animal-welfare-during-transport). The most recent guidance follows Standing Committee of the European Convention for the Protection of Animals Kept for Farming Purposes (T-AP), 2005). Owing in part to the large range of species covered, the guidance requires secondary information in order to be effective, i.e., “appropriate training of stock-people and the use of professional advice on species-specific requirements”, and limited in specificity (containing terms such as: “where possible, pH shall be kept stable”, “it is essential that carbon dioxide levels are kept low”, “enclosures should be regularly cleaned”. The standing committee report recommended “research on the development of husbandry systems, which fully respect the biological needs and welfare, including health, of fish”, with specific areas to target, such as pain perception and food deprivation.

Sources of information for pet owners signposted by (King, 2019) (Assistant chief executive of the Ornamental Aquatic Trade Association (OATA) Ltd., UK.), include OATA, www.thepetcharity.org, and www.practicalfishkeeping.co.uk.

3.1. Cichlids, Cichliformes

a) Behaviour

Cichlid species are the focus of fundamental ecological research into aggressive behaviour (e.g., Nijman and Heuts, 2011; Alward et al., 2021). Cichlids are territorial and fight for dominance, after which overt aggression is much reduced. Social defeat is known to be acutely stressful for subordinates (Sloman et al., 2001), but the longer-term effect on welfare of being housed with a dominant conspecific is not known.

b) Housing requirements

Contrary to the expectation that enrichment would lead to greater territorial aggression, the presence of enrichment can reduce aggression in a resident-intruder test (Nijman and Heuts, 2011). Chemical communication is important for the maintenance of stable dominance relationships, and even replacing only 25% of tank water is enough to elicit aggression between freshwater angelfish, Pterophyllum scalare, and replacing 50% of tank water resulted in an increased in aggression lasting over 24 hours (Gauy et al., 2018).

c) Mortality

Concerns about the mortality of fishes in transport were reported in the interim report. Mass mortality events may be caused by pre-transport infection with gastrointestinal parasites (Enterogyrus sp. and Aeroomonas jandaei) (Assane et al., 2021) in combination with transport stress.

Summary: Cichlids, Cichliformes

Biological or behavioural needs which are difficult to provide in captivity.

• The breeding and transport of cichlids exposes them to a range of risk factors for poor welfare, of which handling is the most stressful component.
• The social environment is another potential source of welfare problems, and owners must be cautious of disrupting stable relationships when introducing new fish or during routine cleaning.

More information is needed to understand the welfare of this animal.

• The welfare of cichlids has been investigated in laboratory studies, but the conditions of cichlids in the pet trade and in private ownership is much less reported.

Key resources

Less water renewal reduces effects on social aggression of the cichlid Pterophyllum scalare (Gauy et al., 2018)

3.2. Clownfishes

a) Capture and breeding

It is estimated that 90% of all clownfish (Amphiprion spp. and Premnas spp. ) are bred in captivity (King, 2019). Fears that children’s films featuring clownfishes increased demand for wild-caught clownfishes were not substantiated by research, and a similar claim regarding blue tang fish, Paracanthurus hepatus, was also shown to be unfounded (Veríssimo et al., 2020). Breeding clownfishes successfully involves a thorough understanding of the breeding structure of wild groups and several search results were related to clownfish reproduction (Fobert et al., 2019; Phillips et al., 2020). Amphiprion ocellaris is protoandrous and its social environment determines the sex of group members. Several articles focused on factors affecting sex determination (Iwata et al., 2008; Iwata and Manbo, 2013; Phuc Thuong et al., 2017; Iwata et al., 2019; Iwata et al., 2019). Clownfish social groups centre on a host sea anemone. Monogamous pairs are collected for breeding. When mated pairs are not available, mixed groups, including sexually immature groups, of fish can be collected and breeding pairs will form. The sea anemones, with which the clownfishes are associated, also need to be transported, and should be kept in separate transportation containers (Madhu et al., 2006). Red Sea clownfish (Amphiprion bicinctus) is one of the most commonly exported ornamental fish from Saudi Arabia, as is Clark’s anemonefish (Amphiprion clarkii) from Sri Lanka (Wood, 2001).

b) Conditions in commercial premises

Husbandry studies often focus on productivity and profitability as outcomes, without mentioning or measuring welfare per se (Chambel et al., 2015). Stress is considered to contribute towards poorer survival in fish (Sharm and Chakrabarti, 1998) and researchers may assume that where growth and survival are depressed, welfare is also likely to suffer. Stocking density has a significant influence on the survival of juvenile clownfishes measured over the course of four months (Chambel et al., 2015). In this laboratory study, survival was 100% when the stocking density was 0.5 fish per litre, and as low as 82.5+/-1.9% at densities up to three fish per litre (survival values were not stated for 1, 2 and 3 fish per litre). Higher stocking densities also depressed growth, with significant decreases in length and specific growth rate. Varying the type of commercial diet fed to the fish did not significantly decrease their survival rate over a four-month study period, running parallel to the stocking density trial. However, the survival rate of fish in the nutrition trial was as low as 68.89+/-2.22%, whereas when only stocking density was varied, fish received a mix of all four diets. In the nutrition trial, stocking density was one fish per litre, which might indicate that individual commercial diets are in some way insufficient to meet their full nutritional needs. In a laboratory study, survival of larvae from hatching to 13 days after hatching varied from 60 to 66% (Nass et al., 2016).

c) Nutrition

The nutritional needs of marine ornamental fishes are less well studied than those of fishes farmed for food, and the complete diets available are not tailored to the needs of particular species (Craig et al., 2017; Vargas-Abúndez et al., 2019). Clownfish larvae differ in their ability to consume large prey from a young age. Clark’s anemonefish is particularly precocial and when fed brine shrimp nauplii from day two post-hatching, and began to metamorphose one day sooner than when feeding commenced on day four or six (Nass et al., 2016). Under laboratory conditions, 300 juvenile Amphiprion ocellaris were fed four different diets for 106 days, including a novel insect diet, black soldier fly, Hermetia illucens , larvae and all survived for the duration of the study (unless sacrificed for analysis), (Vargas-Abúndez et al., 2019).

3.3. Siamese fighting fish

The welfare issues facing pet Siamese fighting fish, Betta splendens, have been reviewed by (Pleeging and Moons, 2017) and are summarised here. A review of stress and welfare in ornamental fishes (Stevens et al., 2017) provides a suggested list of further research priorities.

a) Behaviour

Behaviour-based welfare indicators are lacking, but the building of bubble nests by males is considered to indicate that the water temperature is sufficient. Males are highly competitive and territorial, and housing males together may result in fatal aggression.

b) Housing requirements

Betta splendens is adapted to living in warm water, with a low pH and low oxygen saturation; they have a high tolerance to oxygen levels as low as 0-2 ppm. Species-specific sensitivity to ammonia due to waste products is unknown. Therefore, assessment of water quality, and procedures for water filtration and cleaning for hobbyists are based on recommendations that are not substantiated by the scientific literature. As a result, fish may be inadvertently subjected to toxic effects of high doses or chronic exposure to inappropriate conditioning products.

c) Nutrition

Betta splendens is carnivorous, feeding on mosquito larvae in its natural habitat. Experimental evidence has shown that feeding animal proteins is important for growth, although plant proteins are less risky for introducing mycotoxins. Amount as well as quality of protein is important, with an optimum protein level for young fighting fish of 31-35% protein. Overfeeding leads to deterioration in water quality. The nutritional needs of adult Betta splendens are not well understood and more guidance is needed.

d) Health and disease

The relationship between disease and welfare, particularly infection with Mycobacterium spp., is not clear. Mycobacteria are prevalent in B. splendens and often isolated from dead and dying fish (Zanoni et al., 2008), but it is not known if they are the primary cause of disease, or if infection is only secondary to poor health.

3.4. Koi carp

Most of the published literature on Koi carp, Cyprinus rubrofuscus, found on the Web of Science, using the search terms relevant to this review, concerned viral infections (25 of 47 results). A review of the welfare of common carp, Cyprinus carpio, was carried out by the European Food Safety Authority (Algers et al., 2008). Koi carp can be used in hydroponics (e.g., the production of cannabis) in a dual system, where fish are used as a cheap source of nitrites (via bacterial filtration) (Love et al., 2014). The long lifespan of Koi carp make them attractive due to the reduced need for restocking and associated biosecurity concerns (Maitland et al., 2022).

a) Transport and handling

Netting, grading and transport are stressful events, and the best way to reduce stress is to expedite these procedures. Stressful procedures increase respiration rate and oxygen demand, which can cause acute stress and asphyxia, e.g., at harvesting (measured in rainbow trout, Oncorhynchus mykiss (Van Raaij et al., 1996). Sudden changes in light intensity and spectrum during harvesting, grading and transport are potential welfare issues. To maintain water quality during transport, measures already undertaken are: “(i) addition of atmosphere of pure O₂, (ii) ammonia neutralization or removal procedures, (iii) addition of buffers to the water, (iv) pre-transport fasting, (v) addition of salt or seawater dilution to reach isosmotic salinity, (vi) reduction in temperature, (vii) use of anaesthetics and (viii) addition of probiotics.” Grading is stressful and it is recommended to only grade common carp twice a year (Algers et al., 2008). Feed restriction prior to transport may reduce resilience to stress, increased competition and aggression (studied in salmon, although not in carp), and hunger is a welfare issue in itself. In an addendum to Algers et al. (2008), Broom highlights that assessments of welfare commonly used by producers are incomplete and only take into account growth, feed intake and mortality. Representative sampling of individuals is advised to assess fin damage, health status and the effect of exposure to repeated stressors (which may include changes in light or pressure), to gain a greater understanding of chronic stress.

Long transport duration is associated with extreme elevation in pH due to excretion of ammonia. Oxygen can be supplemented more easily to avoid hypoxia. Additional water quality issues include concentrations of NH₃, NO₂, NO₃, pH, dissolved oxygen and CO₂.

The use of metomidate (a tranquiliser that inhibits enzymes involved in cortisol and aldosterone synthesis) to reduce transport stress (and increasing saleability of the fish after being transported for 24 hours) was evaluated. Outcome measures were: Plasma cortisol and glucose, appearance (graded from 1-5, where lower grades were awarded if fish had severe fin damage, hyperaemia, clamped fins and/or scale loss) and behaviour (graded from 1-4 where negative “behaviours” were rapid respiration, hiding and loss of buoyancy). Neither transport nor metomidate influenced behaviour scores, whereas at the higher doses of metomidate (3.0 and 4.0 mg/L) an increase in cortisol, following transport, was not observed. Koi carp treated with 0 or 4.0mg/L metomidate had significantly worse appearance, so that intermediate doses (3.0mg/L) were recommended. The authors acknowledge that inhibiting cortisol may not reduce stress, but rather the ability to respond to stressors (Crosby et al., 2010).

b) Behaviour

In polyculture, koi carp can attack the eyes of goldfish, Carassius auratus (Oladi et al., 2017), causing obvious negative welfare, but the literature search did not find any concerns quantifying aggression or fin damage between koi carp. The effect of human presence on koi carp is an important factor in their welfare as pets, yet the human-animal bond is poorly researched in fish. Koi carp (seven adults) in an aquaponics learning centre were studied, after an initial period of habituation and handfeeding, to determine whether they would voluntarily interact with humans. The study also sought to understand whether these interactions vary according to individual personality differences or could instead be driven by a general fear of humans or general attraction towards novelty or disturbance (Fife‐Cook and Franks, 2021). Fish voluntarily approached and stayed near to the person’s hand when it was in the water, and individuals varied in their preference to be near the human. However, the carp spent more time close to the human hand in sessions before they had been fed than 20-30 minutes afterwards, so these results could be due to fish associating human hands with the presentation of food rather than any sense of social interaction. Nevertheless, it demonstrates that koi carp can learn to perceive humans positively. Domestic strains of carp appear to be less efficient at consuming live, swimming prey, and less cautious and slower to attack prey. Domestic strains were also more likely to be found in the upper layers of the water than the feral carp, which inhabited the bottom of the water column. These findings suggest that koi carp are adapted to living around humans and being provided with food (Matsuzaki et al., 2009) and that domestic strains which escape captivity are at a disadvantage compared to wild strains, even if the environment is favourable.

c) Conditions in commercial premises

Increasing stocking density (2.8kg/m³) of koi carp fingerlings in an aquaponic system negatively affected growth and body length, and increased catalase activity, and levels of glucose and cortisol, compared with fish kept at 1.4kg/m³ (Nuwansi et al., 2021). Carp are able to tolerate a wide range of temperatures, but enter a state of torpor at colder temperatures (Algers et al., 2008). Often a minority of carp will grow exceptionally fast and become larger than the rest of the population (“shoot carp”), leading to a right-skewed distribution and potential welfare issues, including cannibalism in juvenile populations (van Damme et al., 1989) and smaller individuals suffer because they are outcompeted for food (Barki et al., 2000). In a study of koi carp used in a hydroponics system, the presence of “shoot carp” was not affected by stocking density, average fish weight, cohort size, feed rates, feed-conversion rate or specific growth rate (Maitland et al., 2022). High levels of food competition are thought to encourage shoot carp and a narrow range of sizes may increase competition, whereas adding some larger individuals may dampen the propensity for future shoot carp to emerge. Interestingly, no aggression or cannibalism was observed despite the appearance of shoot carp in every group (Maitland et al., 2022). It may be argued that grading is an ineffective way of preventing the negative consequences of food competition and improving feed provision may be a better focus to resolve the problem of smaller individuals losing out.

d) Health and disease

Cyprinid herpesvirus 3 (cyHV-3), which causes koi herpesvirus disease (KHVD), commonly affects farmed and wild carp (Bocklisch et al., 2006; Negenborn et al., 2015), leading to mass mortality events (Garver et al., 2010; Rahmati-Holasoo et al., 2021; Tolo et al., 2021). The virus is imported into the UK via the ornamental pet fish trade (Wood et al., 2022) and is spread via direct contact prior to the symptomatic phase of the disease (Tolo et al., 2021). Below water temperatures of 16°C the disease is suppressed (Yuasa et al., 2008), but the virus may persist in a latent state after recovery from clinical illness. Koi carp are most at risk of contracting and spreading the disease, if they are mixed during exhibitions and at mating periods (Uchii et al., 2011). Another important cause of mortality is carp oedema virus (CEV) (Lovy et al., 2018), and co-infections with cyHV-3 and CEV can occur in carp populations (Padhi et al., 2019; Sauerwald et al., 2020; Toffan et al., 2020; Tolo et al., 2021).

Other important diseases identified in this review affect the swim-bladder. Inflammation and mortality can be caused by bacteria, such as Proteus hauseri (Kumar et al., 2015), Aeromonas hydrophilia/ caviae group and Shewanella xiamenensis (Sirri et al., 2020), Spaerospora dykovae (Chang et al., 2016) and a range of other bacteria, have been isolated from koi carp suffering from “sinking disease”, including P. aurigonosa and streptococci (Yasumoto et al., 2021). Trichodina mutablis (a protozoan) and Dactylogyrus sp. (gill fluke) may not be primary causes of mortality, but can heavily infest ill fish or those kept in poor environments (Kritsky and Heckmann, 2002). Fish lice (Argulus spp.) can infect fish, even when kept in ponds considered within the recommended range of water quality by veterinarians (Mayer et al., 2013), and can be effectively treated with lufenuron.

Importations of live fishes from non-EU countries should be issued with aquatic animal health certification, pertaining to the supplying country’s disease status. These certificates require inspection within 72 hours of loading, with no clinical signs of disease, and must originate from a country or area which is free of KHVD (among other notifiable diseases), or be subject to quarantine. Importers are required to demonstrate a biosecurity measures plan.

The incidence of internal tumours (neoplasia) in koi carp, examined in Switzerland (belonging to 353 keepers), was affected by husbandry (Knüsel et al., 2015). Higher risks were associated with indoor/outdoor systems (rather than indoor only), larger ponds (although this may be conflated with larger, more expensive fish being more likely to receive veterinary attention), keeping more than 20 koi carp per pond and increased use of praziquantel, formalin/malachite green and potassium permanganate.

The search term “koi carp” and “pain” yielded a single result (Harms et al., 2005), which investigated behaviour as an indicator of post-surgery pain (and the efficacy of analgesia provided intra-operatively). These indicators included general activity level (caudal-fin beat rate), speed of response to feeding (visually orienting towards and consuming pellets of food) and vertical position in the water column. Studies citing Harms et al. (2005) included an experiment comparing two opioid analgesics in koi carp (Baker et al., 2013), which expanded on these behavioural measures, to include “percentage of time fish performed swimming movements in a 2 minute period”, interactive behaviour (orienting towards an observer and food pellet) and hiding behaviour, as well as food consumption and position in the water. Guidelines for the evaluation of pain in koi carp, outside the experimental surgical setting, are lacking. The use of computer vision (using visual images to detect abnormal behaviour in real time) is still experimental (Hümmer et al., 2019), but can identify group behaviour patterns, such as shoaling, feeding, resting, mobbing and hiding.

e) Nutrition

Vijayagopal et al. (2015) investigated the suitability of diets for koi carp, because commercially available diets were not formulated or based on scientific literature on the nutritional requirements of these fish. They specifically investigated the optimum protein (marine protein and soy flour) levels for 150mg koi carp fry, in terms of growth (over 12 weeks) and whole-body fatty acid and amino-acid composition. Diets containing 400-450g protein/kg increased growth rate, compared with diets containing only 250-350g/kg (Vijayagopal et al., 2015). The administration of sodium propionate to koi carp is improved by the use of gelatine micro- and nano-particles, as indicated by several immune system parameters (Sarkheil et al., 2021). Vitamin E supplementation enhanced growth, fertilisation and hatching (Betsy et al., 2021).

Summary: Koi carp, Cyprinus rubrofuscus

Biological or behavioural needs which are difficult to provide in captivity.

• There is some evidence that koi carp are more domesticated (suitable for living around humans) than common carp and they may choose to interact with humans, if handled appropriately.

Evidence of harm associated with captivity.

• The factors which are detrimental to welfare in transport of common carp are likely to also be relevant to koi carp; water quality, handling stress, aggression and food restriction, and mitigation of these requires more research.
• Strategies to manage “shoot carp” (i.e., grading) are harmful and may be ineffective. Adequate stocking density and food availability is important to reduce aggression.
• Use of tranquilisers, which reduce the ability to respond to stressors, may harm welfare and fail to reduce behavioural signs of distress; more evidence is needed.
• Viral diseases, such as koi herpesvirus, are threats to welfare and cause mass mortality, as well as persistent, latent infections. Therefore, improvements in biosecurity are fundamental to improving conditions for koi carp in the pet trade.

More information is needed to understand the welfare of this animal.

• No assessments on the welfare of koi carp in private ownership were found.

Key resources

Standing Committee of the European Convention for the Protection of Animals kept for Farming Purposes, 2005).

Biosecurity and the ornamental fish trade: A stakeholder perspective in England (Wood et al., 2022).

4.0. Reptiles

The reptiles covered in this review are: Ball (royal) pythons, Pythion regius, Burmese pythons, Python bivittatus, bearded dragons, Pogona spp., chameleons, Family Chamaeleonidae, corn snakes, Pantherophis guttatus, garter snakes, Thamnophis spp., green iguanas, Iguana iguana, tegus, Salvator spp., and tortoises, Testudo spp.

Captive reptiles are often considered as a coherent group and statements about their welfare made at the level of Class (Moszuti et al., 2017; Whitehead et al., 2018). Some broad issues are covered, which are common to several reptile species, and then descriptions are given of what is known for the key species targeted in this review. Human health concerns (zoonoses), relating to reptiles as pets, are included in Appendix 1.

The RSPCA commissioned research into the motivations of beginner reptile owners (White and Barber, 2017). The motivation for acquisition of a reptile varied across the key age groups defined by the research, and included media influence (children), a change in lifestyle to becoming able to keep a pet that they had always wanted (20-30s) and being left a pet by a friend or relative that was no longer wanted. Common reasons to give up a reptile included relationship break-up, death of the owner and cost of keeping. Being passed between owners is cited in the RSPCA study as a risk factor for owners being ill-informed about the animals’ histories and needs. Reptiles can be considered easy-to-maintain, hardy pets, which are suitable for people who do not have the space or time to commit to a traditional pet. Respondents felt that they had a lack of information about signs of illness, found information inconsistent (when online sources varied) and agreed that signs of ill-health in reptiles could be difficult to spot; they can look well when they are not.

Onekind (2016) produced a report investigating online adverts of pet reptiles, and whilst this review focusses only on published evidence of welfare harms, it is easily evident from online sales sites that unreliable information is abundantly available. Animals are sold privately as “second hand” rather than going through rehoming centres, thereby missing the benefit of health checks and behavioural evaluations to ensure successful placement (limited evidence from sales sites is given in Appendices 1 and 2).

Warwick (2014) made a strong case against the keeping of reptiles in captivity. Crucially, the severe spatial restriction inherent in keeping reptiles in vivaria is directly responsible for stress-related poor welfare and behavioural expression of this lack of consideration for their behavioural needs. Information available at UK pet stores to reptile owners was reviewed (Williams and Jackson, 2016), highlighting a lack of information about humidity (62% gave no information about humidity requirements and UV light (no seller recommended using a UV light for snakes, only 35% for leopard geckos, Eublepharis macularius, and 80% for bearded dragons)). Although sellers sometimes recommended buying a UV bulb, no further information about the right type of bulb and the need to check and replace them was given.

a) Behaviour

Assessment of new animal-based welfare indicators is made harder by the lack of existing valid, repeatable, and objective indicators against which to validate them. Therefore, testing the preference and the importance of the preference to the individual (Broom, 1988) may be a suitable solution. There is a widely held expectation that it is normal for snakes to be sedentary in captivity (Azevedo et al., 2021) based on the assertion that they are only active in the wild to obtain food, but no longer have the need to explore if their food is provided. In other captive animals, it is acknowledged that providing food, without also providing for the behavioural need to forage, has a harmful effect on welfare (e.g., in parrots, van Zeeland et al., 2013).

On the contrary, Spain et al. (2020a) make the argument that the Madagascar giant hognose snake, Leioheterodon madagascariensis, is morphologically adapted to root through leaf litter for prey, and therefore that burrowing is an important part of its behaviour. Behaviours indicating negative and positive effects in reptiles are listed in Warwick et al. (2013), based on Warwick (1995). Behavioural indicators of affective state are not well understood, e.g., Augustine et al. (2022) investigated “rate of tongue-flicking” as a putative welfare indicator in snakes, based on the premise that this behaviour is associated with increased alertness, which is energetically costly.

There are few experimental studies, which have evaluated the change in behaviour in reptiles after a change in environment or exposure to novelty (Bashaw et al., 2016; Moszuti et al., 2017; Londoño et al., 2018; Spain et al., 2020b; Hoehfurtner et al., 2021; Hollandt et al., 2021).

b) Veterinary care

The use of standardised questionnaires to collect an individual reptile’s history is recommended (Mitchell, 2010), but the collection of a detailed history from owners may be thwarted by the causal acquisition of animals over the internet and where individuals have had multiple previous owners, despite the necessity for owners to record and/ or remember detailed relevant information about the reptile’s current and previous living circumstances. The use of appropriate restraint is important to avoid injury to veterinary staff as well as the reptiles and their owners. Physical examination can be carried out following a checklist, but abnormalities can be missed by those not familiar with the species they are handling. Access to veterinary services for those owning exotic pets is an issue identified a study in the Republic of Ireland, which compared owners of exotic pets (32 respondents) with other types of pet (83 respondents) (Goins and Hanlon, 2021a, 2021b). Only 50% of exotic pet owners consulted a vet in 2019. Comparable figures were not provided for other domestic species, however the PDSA “Pet animal wellbeing” report stated that in the same year, 78% of dog owners and 61% of cat owners said their pet had regular booster vaccines (implying at least annual veterinary health checks) (PDSA, 2019).

In a review of diagnosis and management of disorders of the digestive system (Mans, 2013), plain radiographs were of limited use, and contrast radiography is recommended, although barium sulphate is associated with significant risks and iodinated contrast media should not be administrated to dehydrated animals. Ultrasonography can be a useful tool in the detection of ileus (a condition in which the intestines do not move correctly), with a possible risk of misdiagnosis due to the slow transit time of the normal reptile gastro-intestinal (GI) tract. Disorders of the periodontal cavity may be more amenable to diagnosis by less specialised veterinary surgeons, and prevalence of dental disease is around 50% in UK bearded dragons (Mott et al., 2021). Inappropriate diet (containing fruit), over- and underweight animals, and poor husbandry are identified as the main risk factors for dental disease. The high prevalence of dental disease in bearded dragons (cf. UK dog population (12.5% prevalence of disease in a study of 22,333 dogs (O’Neill et al., 2021)) is related to poor husbandry

4.1. Squamates

4.1.1. Ball (royal) pythons

Warwick (2014) raises the following concerns about the welfare of Python regius kept as pets. Ball pythons are nocturnal/crepuscular and particularly subject to photo-invasive environmental stress. They require complex naturalistic environments, and consideration of the following: space, temperature, chemical cues in the artificial environment, diet and nutrition, handling stress, veterinary medical issues, captivity-stress-related behavioural problems, interaction with transparent boundaries, hyperactivity, hypoactivity, disposition-related voluntary hypothermia, social stress, and behaviour-related self-injury and disease. No studies were identified, which measured transport stress in this species. The absence of information about the welfare of wild-caught and ranched snakes is highlighted by Green et al. (2020).

a) Capture or breeding

Two recent reviews have been published on the topic of ball python welfare (D’Cruze et al., 2020; Green et al., 2020). The welfare of ball pythons at expositions around Europe and North America, including one in Doncaster, UK (28 vendors selling 427 snakes) demonstrate a general failure to meet RSPCA standards (adequacy of mobility/space, shelter, water, substrate and hygiene), but it is not clear how the UK vendor ranks (D’Cruze et al., 2020). Ball pythons, kept as pets, are imported from West Africa, where they are farmed for the pet trade or “ranched” (eggs are taken from the wild and hatched on farms (Green et al., 2020)).

b) Behaviour

FBH (2014) provides broad guidelines for owners to assess the welfare of their animals. The authors recognise that information available on the internet is not always reliable and updated and recommends the source “Reptile & Amphibian Information Portal: http://www.raaip.org.uk” as “constantly kept under review by a panel of experts and updated as appropriate”. Unfortunately, this site no longer exists; searching for “Reptile & Amphibian Information Portal” did not find this source. The good practice guidelines (FBH, 2014) advise owners to watch for the following signs:

“They may hide away, refuse to feed, become restless, aggressive or lose their normal colouration. There may also be direct signs of illness, such as swellings, discharge, breathing difficulty, diarrhoea, sores, weight loss or gain, sensitivity or constipation or problems with dysecdysis (skin-shedding).”

“Behaviour problems can include persistent aggression, escape behaviour (e.g., snout-rubbing), repetitive behaviour and lethargy.”

The size of housing for ball pythons, which may live up to 20 years, is a source of debate. The RSPCA care sheet states “A royal python needs a vivarium which allows it to fully stretch out.”(RSPCA, 2019b). The lack of published evidence, describing how snakes experience their captive environment, is highlighted in a review of evidence for reptile sentience (Lambert et al., 2019).

c) Conditions in commercial premises

A rack system is often used for pythons, with shelves and bins arranged as drawers (Hollandt et al., 2021), with heat provided in the form of pads or cables. This system is usually sparse and contain a hiding place and water bowl, with newspaper, rodent litter or bark mulch as litter. They may also contain artificial plants, tree branches and a basin to provide the opportunity for bathing. There is concern from experts that this set-up does not provide for the full behavioural repertoire of pythons, e.g., hiding in various places, climbing, burrowing and lack of adequate light provision. Where opportunities are provided in a terrarium, bathing, basking and climbing were expressed by ball pythons (Hollandt et al., 2021). In contrast, racks may increase feeding, and therefore growth and earlier reproduction. The rack system was associated with greater abnormal behaviour (pushing the mouth against a barrier) and more time resting in the hiding place than in a terrarium. The behaviour “resting outside of the hiding place, stretched out” tended to be more common in terraria. Ten snakes in the rack system pressed their snouts against the rack system and appear to try and widen them using burrowing movements. This behaviour was not displayed when they were returned to terraria after the experiment. No difference in feed refusal was found between housing systems. Therefore, it is concluded that the rack system is not appropriate housing (Hollandt et al., 2021).

d) Nutrition

Pythons may refuse to eat dead prey and therefore feeding of live rodents is the only alternative (Hollandt et al., 2021). No other articles on nutrition of ball pythons were found.

e) Health and disease

Evidence of insufficient hygiene and litter standards is prevalent in videos of ball pythons in commercial premises (D’Cruze et al., 2020). A large exotic pet breeder in Texas, USA was investigated in 2013 and the conditions were found to be catastrophic (Ashley et al., 2014), with extremely high levels of mortality (“3,500 deceased or moribund animals (12% of stock), mostly reptiles, were discarded on a weekly basis”) associated with improper housing and husbandry, (deaths in snakes were due to trauma, caused by overcrowding, crushing, fighting, damage due to improper handling and cannibalism), infections, dehydration, emaciation, and hypothermic stress.

This “spider head shake” is a genetic disorder of the central nervous system, which occurs in “spider ball snakes” as a consequence of selection for their colouring. Rose et al. (2014) reviewed the evidence for welfare costs associated with uncontrolled muscle spasms and muscle weakness, which occur due to this condition, particularly around feeding. The review concludes that although this is perceived as frustrating and uncomfortable, more research is needed to understand the experience of snakes affected by this condition. However, “freedom from disease” is a central component of animal welfare and relevant to welfare legislation protecting animals from suffering.

Ball pythons appeared in two studies relevant to their emotional experience, but welfare assessment did not investigate this (one study of “wobble” syndrome concluded that this deformity was likely to be frustrating for “spider morph” snakes (Rose and Williams, 2014)). Not being able to perform a motivated behaviour, such as feeding, could be defined in a functional sense as frustration, but it is not known if these snakes suffer associated mental distress. The second example uses delayed feeding as an indicator of pain (James et al., 2017). The treatments, which provoked this behaviour (chemical noxious stimulus or surgical incision), are known to activate pain pathways in afferent nerves (C-fibres), and surgical incisions, which cause tissue damage in tissue supplied by afferent nerves, are a recognised source of pain.

4.1.2. Burmese pythons

The Web of Science search found only two relevant articles on Burmese pythons, Python bivittatus; a report on mites in pet Burmese pythons in Malaysia (Mariana et al., 2011) and evidence for a positive effect of UVB radiation over 10 months in a zoo population (Ouwehand Zoo, Netherlands) on vitamin D-3 synthesis (Bos et al., 2018). In the Journal of Exotic Pet Medicine, Burmese pythons are mentioned in the articles “Selected infectious diseases of wild reptiles and amphibians”, (Schumacher, 2006b) and “Urinary tract diseases of reptiles” (Reavill and Schmidt, 2010).

Inclusion body disease is associated with high morbidity and mortality in captive snakes. The symptoms of this disease in pythons are neurological (incoordination, failure to right themselves from dorsal recumbency) and are incurable. The route of transmission and aetiological agent are not completely clear, although the snake mite, Ophionyssus natricis, is considered a vector (Schumacher, 2006a). Ophidian paramyxovirus (OPMV) is present in captive boid snakes, but may be asymptomatic. Symptoms include loss of appetite, respiratory tract disease and, in extreme cases, seizures. Transmission is likely via respiratory secretions and no treatment is available.

Information on welfare of pet Burmese pythons was not evident in the literature, although these animals are available for sale online (see Appendix 2). Changes in circumstances and no longer having space are reasons cited for selling Burmese pythons. The welfare impact of relinquishment/ changes in ownership over the lifespan of these pythons has not been studied.

4.1.3. Bearded dragons

a) Breeding

Bearded dragons, Pogona spp., in the UK are bred in captivity and breeders import animals from Europe and the USA (e.g., “dragonmorphs.co.uk”). Siviter et al. (2019) found that hot-incubated bearded dragons had slower growth, but were faster at completing a cognitive task and completed it more often than cold-incubated bearded dragons. The hot- and cold-incubated bearded dragons were placed in novel-object and novel-environment tests, and there was no consistent difference in behaviour according to treatment (Siviter et al., 2017).

b) Transport and handling

No literature was found on the welfare of bearded dragons in commercial settings or in transport. To evaluate the effect of handling duration on the welfare of bearded dragons, three conditions were tested in 13 captive-bred lizards, including less than one minute transfer between rooms, five or fifteen minutes of gentle, calm handling by an experienced handler over a period of four days per week for three weeks (Stockley et al., 2020). In a subsequent novel-environment test, bearded dragons which had been handled for 15 minutes demonstrated more tongue flicks than those that were carried for < 1 minute. Minimally handled animals also spent more time close to a novel object than those handled for five minutes, while the 15-minute treatment was intermediate. The authors referred to previous studies of bearded dragons in novel-object and novel-environment tests (Moszuti et al., 2017; Siviter et al., 2017) and concluded that their results (more tongue flicks, less time close to the novel object) indicated aversive or anxiety-like responses to handling (Stockley et al., 2020), despite neither of the former studies demonstrating an association between behaviour in the test arena and any other measure of stress or affective state. The lack of validation between measures so far limits the use of novel-object or enrichment tests, or tongue-flicking as indicators of anxiety in bearded dragons. However, tongue-touching could be used to indicate bearded dragon’s sensitivity to changes in their environment (individuals may increase or decrease in their responsiveness to novelty according to health or energy status), or to assess the effectiveness of an enrichment item in stimulating exploration.

c) Behaviour

To assess response to novelty as a possible marker of anxious or fearful personality, bearded dragons were presented with a novel or a familiar environment (different substrates: bubble wrap or saw-dust and different wall patterns were used as contextual cues). Behavioural responses to novelty included locomotion, elimination, latency to approach the novel object and reptile-specific measures, such as “tongue-flicks directed into the air (air-flicks) and tongue-flicks making direct contact with a surface (tongue-touches)”. Bearded dragons performed more tongue-touches in the novel compared with familiar environment, but the same number of air-flicks (Moszuti et al., 2017). Tongue-flicking in response to a change in environment is an exploratory behaviour, used to sample chemicals from the environment (Cooper, 1994). This behaviour did not correlate with other measures of response to novelty (latency to move, defaecation).

d) Housing requirements

Vergneau-Grosset and Péron (2020) reviewed the effect of UVB light exposure on vertebrates. In contrast with results for other vertebrates, artificial UVB lights enhanced vitamin D production in bearded dragons to a greater extent than natural sunlight (Kroenlem et al., 2011). However, a short lapse in UVB provision is unlikely to be harmful for adults, because the concentration of calcidiol and calcitriol can remain stable for over two months without UVB exposure (Oonincx et al., 2013). UBV exposure is more effective than oral vitamin D3 supplementation in increasing plasma calcidiol, but low serum calcidiol and calcitriol promote the consumption of vitamin-D-rich foods by bearded dragons (Oonincx et al., 2010).

e) Health and Disease

A review of mortality in 36 bearded dragons necropsied at pathology facilities in New York, USA (Crouch et al., 2021) described the most common causes of death as inflammatory (69%) and chronic/degenerative (47%) (N.B. multiple causes were counted in more than one category). Common findings included systemic illness, such as coelomitis and bacterial sepsis, chronic liver disease and hepatitis, pneumonia and chronic nephritis. Crouch et al. (2021) did not evaluate the causes of disease. A review of cases presented to a university diagnostic imaging department (Lublin, Poland) found that most bearded dragons were presented for physical changes, deformities, weight loss and inappetence. It is likely that skeletal and coelomic presentations are most commonly represented here because more superficial conditions would not require imaging, but the prevalence of musculosketal injuries (29.33%), both traumatic and developmental deformities, suggests poor bone strength is an issue in this population (Łojszczyk-Szczepaniak et al., 2018). Moszuti et al. (2020) and Gimmel et al. (2017) identified choleliths as surprisingly commonly found at necropsy in Germany, which may indicate an increasing trend.

Nutritional secondary hyperparathyroism is common in reptiles in North America and calcium metabolism is also a common cause of constipation due to the role of calcium in gut movement (Wright, 2008). Analysis of bearded dragon clinical cases in Austria and Hungary identified parasitism as a common contributor to gastrointestinal disease, “In 51.92% of the cases of constipation, endoparasites were present, whereas in 38.46% of the cases of constipation, metabolic bone diseases and imbalances in calcium and phosphorus levels were detected”. No similar large case reviews were found in the UK bearded dragon population (Schmidt-Ukaj et al., 2017).

4.1.4. Chameleons, Family Chamaeleonidae

There is no “RSPCA Care Sheet” for chameleons, nor AZA (Association of Zoos and Aquariums) animal care manual nor EAZA best practice guidelines. Breeding in captivity is described as relatively easy and successful in veiled chameleons, Chamaeleo calyptratus (Diaz et al., 2015), compared with other reptiles within a laboratory setting.

a) Housing requirements

UVB is recommended for panther chameleons (Furcifer pardalis); the optimum levels have been defined in terms of reproductive success (290–315 nm), and due to their ability to self-regulate exposure to UVB depending on their vitamin D status, a gradient is recommended (Watson and Mitchell, 2014). Short exposure to high irradiation was not found to be equivalent to longer exposures at mid-low UVB light levels (5–15 mW/cm²) (Ferguson et al., 2002). A study of UVB lights in a Hungarian veterinary journal, “Magyar Allatorvosok Lapja” (abstract available in English) stated that popular brands of UVB lights, labelled as effective for one year, lost 50% of their irradiation by the 14^th week (Nikoletta and István, 2018).

b) Nutrition

Metabolic bone disease can occur due to nutritional deficiencies in vitamin D, vitamin A and calcium, and prevention involves provision of long-low UVB exposure (3–120 μW/cm^{2 10h/d})^, feeding of insects, gut-loaded with 12% Ca and dusted with 75mg/kg vitamin A and 0.625mg/kg cholecalciferol (Hoby et al., 2010).

c) Health and disease

Infectious diseases reported in chameleons include viruses: Novel herpesvirus (Hellebuyck et al., 2021); iridovirus (Weinmann et al., 2007); ranavirus (Peiffer et al., 2019), endoparasites (nematodes, (Orós et al., 2002); trematodes, (Collicutt et al., 2017); ascarids, (Reitl et al., 2021)), are mostly single-case reports. A study of Chamaeleomyces g ranulomatis fungi in veiled chameleons (Chamaeleo calyptratus) in a zoo in Germany suggested this disease is common and fatal (Schmidt et al., 2012), but the route of infection was not established. Parasitic infections in captive chameleons are described as common and guidance on treatment is provided (Stahl, 1997, USA), but no recent reviews on the prevalence of infectious disease in UK captive chameleons were found. Antibiotic resistant Salmonella can be isolated from captive veiled chameleons (Barazorda Romero et al., 2015).

d) Mortality

In a study of captive reptile mortality rates in the home (Robinson et al., 2015), a figure of 28.2% mortality within the first year of acquisition was found for chameleons. This figure was a result of randomised-response technique and direct questioning, rather than directly acquired from records and the two methods did not differ significantly in their results. The direct questioning method included the question: “Of the X that you acquired over the last five years, how many died within 12 months of acquisition” and was posed to a sample of attendants at two large meetings for reptile breeders. The breeders also responded to the survey that, based on their own experience, chameleons were “very difficult/ difficult to keep” (41% of respondents), compared to 28.2% rating them easy/ very easy to keep. Panther chameleons have a short lifespan in the wild (less than one year, (Andreone et al., 2005), and, therefore in this specific case, the figure of 28.2% chameleons dying within a year of acquisition may not truly reflect poor husbandry. Labord’s chameleon (Furcifer labordi) is short-lived; 4-9 months in the wild (Eckhardt et al., 2017).

4.1.5. Corn snake

Corn snakes, Pantherophis guttatus, were the most relinquished snake to the SSPCA (2016- 2020). However, few health, welfare or behaviour issues were reported in the literature.

a) Behaviour

Corn sakes are solitary in the wild and can be kept as single pets. Environmental complexity (beyond the standard enclosure, which contained a rock/cave hide and newspaper substrate and a small water-bowl) increased active behaviour in a study of 15 adult corn snakes, which showed a significant preference for an enriched vs. standard side of an enclosure (Hoehfurtner et al., 2021). A clear preference is also demonstrated for larger enclosures, in which snakes can fully stretch out compared with an enclosure only 2/3 their length. (Hoehfurtner et al., 2021). Corn snakes are obligate carnivores and captive adult snakes are fed on dead (fresh, or frozen and thawed) rats and mice.

b) Health and Disease

A case report of Kalicephalus hookworm infection was reported in four corn snakes in the USA (Matt et al., 2020) and a single case of arteriosclerosis, leading to arterial rupture and acute death in a corn snake (P. guttatus guttatus), was diagnosed also at a North American veterinary clinic (Zellar et al., 2019). No other articles in the Journal of Exotic Pet Medicine concerned the health and welfare of corn snakes specifically. Only five articles resulted from the Web of Science search (including Matt et al. (2020)), which may suggest that despite their popularity, pet corn snakes are not regularly presented to veterinarians for health problems.

4.1.6. Garter snakes

The RSPCA produces a care sheet for pet garter snakes, Thamnophis spp. Garter snakes are diurnal, highly active and non-venomous (RSPCA, 2019a). Captive garter snakes have smaller heads than wild snakes, which limits their ability to catch prey and survive if released into the wild (Ryerson, 2020). Captive garter snake welfare in the UK was not represented in any search results in Web of Science.

Corticosterone can be assayed as a biomarker of stress, which increases immediately after handling in garter snakes, particularly in wild-caught snakes (Aldridge and Arackal, 2005) and was shown to differ in populations from different locations, with the stress response decreasing in older snakes (Gangloff et al., 2017). Snakes collected at different times of year also differ in their glucocorticoid levels (Dayger and Lutterschmidt, 2016). Corticosteroid is not repeatable over time within individuals, and not shown to correlate with heterophil to lymphocyte ratio (a common measure of white blood cell stress response (Sparkman et al., 2014)).

4.1.7. Green iguanas

Faecal metabolites of cortisol reflect the level of stress experienced in captive green iguanas, Iguana iguana, and this is increased by handling and living in an environment, which does not provide them with the opportunity to climb (Kalliokoski et al., 2012).

Most studies fall into the category “health and disease”, but most conditions have a link to poor husbandry, which are commonly nutritional deficiencies. In common with other captive reptiles, green iguanas suffer from metabolic bone disease. The condition may not be diagnosed until it is severe and difficult to reverse, therefore Zotti et al. (2011) developed methods to improve diagnosis, using radiography to analyse bone density. Similarly, novel methods to monitor metabolic disease (plasma protein electrophoresis) were successfully trialled. This technique was more effective in hepatic and renal disease than skin disease, since the systemic diseases were more likely to result in a decrease in albumin:globulin ratio (Knotkova et al., 2019).

Treatment of cryptospirosis can be achieved using potentiated sulphonamides or halofunginone. However, both groups were administered intravenous fluids and hyperimmune bovine colostrum. Therefore, to avoid euthanasia due to the pathology caused by cryptosporidium, intensive in-patient care may be required (Gałęcki and Sokół, 2018). Skin diseases are often caused by poor husbandry, including hypovitaminosis A and systemic disease, which result in protein loss (hypoproteinaemia), but the underlying causes of common conditions such as dysecdysis (problems with skin shedding) are not fully understood. A variety of infectious causes are described, although since the normal skin flora are not well characterised, diagnosing the underlying cause is challenging (Hellebuyck et al., 2012). (Brown et al., 2006) concluded that mycoplasmas (Mycoplasma iguanae) are unlikely to be primary pathogens in green iguanas and may normally colonise the respiratory tract. Green iguanas are also presented to vets due to burns (from inappropriate heat or light fixtures) and trauma. Management of common emergency presentations, including dystocia, renal failure, sepsis, dyspnoea, gastrointestinal foreign bodies, cloacal prolapse and toxicosis, are described by Wellehan and Gunkel (2004), although a recent indication of the prevalence of these conditions was not found.

4.1.8. Tegus (tegu lizards)

Tegus, Salvator spp., are large, South American lizards, which are available to buy online (e.g., www.bluelizardreptiles.co.uk) and on rehoming sites. However, the Web of Science search yielded only two studies with relevance to their care. Cury de Barros et al. (2010) conducted a laboratory study, which concluded that larger, adult tegus were more aggressive than smaller (juvenile) tegus and that at lower temperatures small lizards showed escape behaviour, whereas large lizards stayed inactive in a defensive posture. The second study describes the treatment of malaria (Plasmodium) infection with potentiated sulphonamide antibiotics. However, these animals were living in Brazil and malaria is not endemic in the UK.

Three articles in the Journal of Exotic Pet Medicine specifically mentioned tegus in the title, two of which were single animal-case reports (multicentric lymphoma, Saldanha et al. (2021) and isolation of antibiotic-resistant Salmonella, Giacopello et al. (2012)). Recommendations for sedation and pain relief (antinociception) of Salvator merianae are given based on a prospective, crossover, randomized study in six captive lizards (Bisetto et al., 2018). An abstract from the American Journal of Veterinary Research (Leal, 2017) was found, which evaluated morphine and butorphanol on limb-withdrawal in tegus, concluding that mu agonists provided “antinociception”. The diagnosis of gastrointestinal foreign bodies in reptiles was illustrated by a case of a perforating foreign body (wooden material from the enclosure) in a red tegu, Salvator rufescens (Mans, 2013).

In a general article describing reptile dermatological conditions, poxvirus is identified as infecting caimans, Family Alligatoridae, and tegus (Hoppmann and Barron, 2007). Lesions can be diagnosed on histopathology and do not require treatment unless secondary infection is present.

Care guides are not published on the AZA, EAZA and RSPCA websites, and owners are likely to rely on internet sources. Care sheets are provided by hobbyist websites, such as Reptiles magazine: Tegu Lizard Housing and Care Information, Reptiles Lounge, Repitlinks and Reptifiles (summarised in Appendix 3).

Reptifiles website provides the most detailed and extensive “shopping list” of equipment required, including UVB lamp, dual lamp fixture with reflector, LED bar, ceiling mount ceramic socket, halogen heat bulb, flagstone for basking, temperature and hygrometers. The approximate cost of buying (without the tegu or food) is estimated at $2,600, although this can be reduced if the enclosure is hand-made. In addition, guidance for inspecting tegus before buying them includes an eleven-point health check.

Information given by hobbyist websites is inconsistent regarding advice on housing tegus socially, e.g., Reptiles lounge: “Their social skills allow them to cohabitate in one enclosure. The only thing you need is to double everything for two and increase accordingly as you add a tegu”, Reptilinks: “Blue tegus may not play well with others, be extremely careful not to keep two males together. If not breeding, keep two females with plenty of space.”, Reptifiles: “Tegus are perfectly happy living alone. Female and female pairs or male and male pairs can be housed together (although individual personalities mean cohabitation won’t always work).”. Only Reptifiles provided any information on enrichment and included more information about potential negative behaviour, including advice that tegus can be trained (to an extent), can run on two legs, can jump almost a metre straight up, go through a “puberty” like adolescent phase during which they are “thoroughly unpleasant to deal with” and even a tame, adult tegu will bite/scratch/ tail whip, if scared or threatened.

No evidence was available on the extent to which inappropriate rearing, or variation in amenity to “taming” creates problems for tegus, in terms of aggression, anxiety, injuries, stress-related behaviour problems, lack of exercise opportunities and/or relinquishment.

Another area of concern highlighted by this guidance is the heat, light and exercise requirements of these lizards, which may be possible to fulfil in some areas of the USA where they are popular pets, but exercise outside, and/ or exposure to direct natural sunlight in addition to artificial UVA/UVB and LED lights is important for their welfare. Weather conditions in Scotland may not be appropriate to fulfil this need.

Summary: Snakes and lizards

Evidence of harm associated with captivity.

• Relinquishment of reptiles with long lifespans is likely to affect their welfare. Even if the reptile’s health and welfare is not the cause of rehoming, it is likely they are not sold to new owners with the level of oversight and information to ensure a successful placement. Following reptiles across their lives is a challenging avenue for research, but more longitudinal studies may help to formulate regulations for the keeping of reptiles (such as record-keeping and checking in with veterinarians), to ensure that long-term harm is not caused unwittingly.

More information is needed to understand the welfare of this animal.

• For all snakes, pythons especially, housing in small tanks does not represent the opportunity to display a full range of normal behaviours, but the lack of evidence on the welfare effects of confinement (e.g., rates of obesity, activity budgets) results in a lack of awareness of what “normal” should look like.

Tegus

Biological or behavioural needs which are difficult to provide in captivity.

• The success of “taming” tegu lizards is likely to be critical to their successful keeping, and the incidence of aggression is not known.
• The climate in Scotland may not be suitable to provide suitable levels of natural sunlight for tegus to supplement artificial sources. Given their size, enclosures, which provide sufficient heat, artificial light and UVB, but also opportunities for exercise and exploration, are likely to extremely difficult to provide.

More information is needed to understand the welfare of this animal.

• There was very little expert advice or published evidence of pet tegu welfare.

Chameleons

Biological or behavioural needs which are difficult to provide in captivity.

• Detailed knowledge on dietary needs for vitamins and minerals, effective heat, light and UVB for commonly kept reptiles may already be sufficient to prevent deficiencies (or excesses), but owners need to be well informed and fastidious about monitoring conditions.

Evidence of harm associated with captivity.

• Chameleons seem to be at a particular risk of premature mortality in the home, which requires more investigation, but natural lifespans must be accounted for.

Key resources (squamates)

Emergent diseases in reptiles (Wellehan and Gunkel, 2004)

Effect of ultraviolet radiation on vertebrate animals: Update from ethological and medical perspectives (Vergneau-Grosset and Péron, 2020)

Good Practice Guidelines for the welfare of privately kept reptiles and amphibians (FBH, 2014)

Royal python care sheet (RSPCA, 2019)

Garter snake care sheet (RSPCA, 2019)

Corn snake care sheet (RSPCA, 2019)

Bearded dragon care sheet (RSPCA, 2019).

4.2. Testudines (tortoises)

4.2.1. Hermann’s tortoise, Testudo hermannii

In the UK, only captive-bred tortoises are legal to keep as pets. A research article from Slovenia (Dovc et al., 2021) on improving the success rate of hatching healthy T. hermannii examined the causes of embryonic mortality, finding that after infertility, infection was the most common finding (52.5%), and infectious agents were: Pseudomonas aeruginosa, Bacillus sp., Purpureocillium lilacinum, and Escherichia coli.

a) Behaviour

Males should be housed singly due to territorial aggression. In captivity, a commonly reported undesirable behaviour is “excessive courtship”, involving sexual and aggressive behaviour directed towards other tortoises. Endoscopic removal of the testicles (orchiectomy) was demonstrated to reduce this behaviour to the extent that tortoises could be housed in groups in 59% of cases (Hatt et al., 2019). In eastern Hermann’s tortoises, Testudo hermannii boettgeri, shell colour was found to predict personality; darker shell patterns were associated with more aggression and boldness in male tortoises (Mafli et al., 2011).

b) Housing requirements

Natural sunlight is important to maintain plasma vitamin D and avoid calcium deficiency. Although Selleri and Di Girolamo (2012) found sunlight to be more effective than mercury-vapour or fluorescent lamps, in the absence of natural sunlight alternative UVB sources, such as those used for other reptiles, could be investigated. A review of the welfare of pet tortoises in Germany was quite optimistic, reflecting owners with a good understanding of the needs of their animals. Most provided the optimum diet and housing (over 75% provided a greenhouse or cold frame with an outdoor enclosure) (Bauer et al., 2019).

c) Nutrition

German tortoise owners mostly provided a good diet (approximately 68% of owners fed a diet, consisting of more than 80% grasses and weeds over summer) (Bauer et al., 2019). Reliable dietary information for owners is available at: www.thetortoisetable.org.uk (Roberts et al., 2017). Both inadequate grass/ weeds and tortoises restricted to a terrarium were at higher risk of pyramidal growth syndrome (Bauer et al., 2019). Morin and Priymenko (2018) suggested that owners require more information on appropriate diets for tortoises, as current recommendations only consider selecting foods with an appropriate mineral balance. Optimum levels of vitamin supplementation were tested and over-supplementation of vitamin E, K, B1, B2, B6 and B12 and biotin, combined with less vitamin D was demonstrated to be detrimental to shell strength. The most successful of the two diets contained 50 000 IU/kg vitamin D and both diets contained similar amounts of calcium (Hetenyi et al., 2014).

d) Health and disease

Protozoal infections can severely affect captive tortoises, and the diagnosis and treatment of the key pathogens (amoebae, ciliates, flagellates, coccidia and apicomplexans) are described  by Bardi et al., 2019). Amoebae infections, in particular, can lead to chronic diarrhoea and dehydration with a poor prognosis. The most effective prevention for protozoal disease is hygiene and biosecurity. Oxyurid nematodes have a very high prevalence in pet tortoises (43.18%) compared with protozoa such as amoebae (0.005%) (Hallinger et al., 2018).

Investigation of a disease in juvenile tortoises, which has symptoms including soft shells and skeletal deformity, stunted growth and abnormalities affecting multiple organs (including the liver and kidney), found that a picornavirus was responsible; more research is needed into this newly characterised virus (Heuser et al., 2014). Tortoises were included in a veterinary article advising treatment of chelonians as in-patients (Norton, 2005) and the successful application of a novel technique for tissue repair was reported (radio electric asymmetric conveyer (REAC)) (Rinaldi et al., 2013).

Summary: Tortoises, Testudines

Biological or behavioural needs which are difficult to provide in captivity.

• Although the welfare of pet tortoises in the UK has not been surveyed recently, results from Germany suggest a recent trend towards improved conditions and suggest it is possible for owners in a similar climate to provide tortoises with a healthy lifestyle.

More information is needed to understand the welfare of this animal.

• Further directions for research, which would benefit pet tortoises include investigating whether owners have adequate information on parasite control, provision of UVB and nutrient requirements.

Key resources

Occurrence of health-compromising protozoan and helminth infections in tortoises kept as pet animals in Germany (Bardi et al., 2019).

Nutrition and husbandry conditions of Palearctic tortoises (Testudo spp.) in captivity. (Bauer et al., 2019).

The Tortoise Table (Roberts et al., 2017).

5.0 Amphibians

Michaels et al. (2014) and Burghardt (2013) draw attention to a lack of research into the behavioural responses of amphibians to captive conditions and appropriate environmental enrichment. Shelter provision increased growth rate in Túngara frogs (Engystomops pustulosus) and substrate was preferred if the frogs could dig (Walsh and Downie, 2005). Since this review was published, a study on enrichment in African clawed frogs, Xenopus laevis, (Ramos and Ortiz-Díez, 2021) was conducted, and these frogs showed a preference for artificial plants (preferred over plastic pipes, and clear space), which supports the findings of Michaels et al. (2014), in finding that plants improve the welfare of red-eyed tree frogs, Agalychnis callidryas, (growth rate, diversity of gut bacteria) and that tree frogs show a preference for plants, especially when deprived of access to plants before the choice test.

5.1. Alpine newt

The wild introduced population of alpine newts, Ichthyosaura alpestris , estimated using photos of alpine newts on social media, is small in Scotland (eight photos identified in total (Allain et al., 2021). No papers were found on the welfare of pet alpine newts.

a) Breeding

Alpine newt larvae are very sensitive to UVB radiation and therefore unlikely to survive in shallow water due to the effect of direct sunlight (Nagl and Hofer, 1997).

b) Health and disease

In wild amphibia, pathogenic fungi, such as Batrachochytrium dendrobatidis, can deplete wild populations and have been detected in some newt species in Germany (Ohst et al., 2013). Batrachochytrium salamandrivorans has caused fatalities in amphibian populations in Europe (in the Netherlands and Belgium). According to a recent paper (Allain and Lynn, 2021), no cases of B. salamandrivorans have yet been reported in wild alpine newts in the UK (Cunningham et al., 2019), but it has been found in a collection of captive newts at the Zoological Society of London (no species information given; Cunningham et al. (2015)). These pathogens are a serious threat to captive and native wildlife, and the use of single-use plastic gloves is necessary to avoid transferring B. dendrobatidis between animals (Thomas et al., 2020).

5.2 Argentinian horned frog, Ceratophrys ornata

There were no results on WoS for “Argentinian horned frog” and of the results for “Ceratophrys ornata”, four articles were relevant for amphibia in captivity or interaction with humans (Secor, 2005; Trudeau et al., 2010, 2016; Deutsch et al., 2021). There are several common names for this type of frog; searching “ornate horned frog” and “pac-man frog” each identified one additional paper; a metabolic study of estivation (Groom et al., 2013) and isolation of an unusual Brucella variant (Soler-Lloréns et al., 2016). The terms “South American horned frog” and “Argentine wide-mouthed frog” did not yield any relevant results.

a) Capture and breedings

Deutsch et al. (2021) investigated the impact of the pet trade on local (Argentine) horned frog populations. In Argentina, Uruguay and Brazil, people who had had contact with the species mostly had negative attitudes towards C. ornata and those with negative attitudes felt so strongly that most (67%) killed the frog when they encountered it. Most frogs owned as pets in this region of South America were wild caught, with the rest mainly from unlicensed breeders or a university facility. Only one licensed breeder of C. ornata was found in Argentina.

Trudeau et al. (2010) tested a new commercial product for the hormonal manipulation of reproduction in captive frogs, finding a potential benefit to welfare using injectable hormones, which required only one injection per individual, reducing handling stress compared with other methods.

b) Nutrition

Secor (2005) conducted an experimental study of the process of aestivation. This is a process by which C. ornata can reduce gut activity during periods without food, and then when fed (rodent meals), they upregulate nutrient absorption, gut mass and intestinal transport rates.

5.3. Fire-bellied toads, Bombina spp.

A contributing factor to this toad’s negative reputation in its native environment and likely unsuitability as a conventional “pet” is the secretion of a toxin, which causes skin irritation in humans (see Appendix 1).

a) Housing requirements

The fire-bellied toad may require UVB in addition to dietary calcium and vitamin D, to achieve optimum skeletal structure. UVB light was demonstrated to enhance serum D3 (Michaels et al., 2015). Although there is a lack of information about metabolic bone disease in the pet population, provision of UVB light may be important for the husbandry of this toad.

b) Health and disease

As with alpine newts, B. dendrobatidis is a risk to health in fire-bellied toads. The prevalence of this pathogen was reviewed  by Berger et al. (2016). Options for treatment are given in Martel et al. (2011).

The understanding of analgesia and anaesthesia is not as far developed in amphibia compared with other animals, and several studies reviewed effective anaesthetics for fire-bellied toads (d’Ovidio et al., 2015; Adami et al., 2016a, 2016b).

5.4. Tree frogs, Family Hylidae

No relevant search results for pet tree frogs were found in the UK or countries with similar pet-keeping practices. No publications were found describing the captive conditions, welfare in transport, handling stress, husbandry, nutrition, incidence of metabolic disease and social behaviour of privately owned tree frogs.

Infectious disease studies were non-UK based, including the detection of ranavirus in a green tree frog (Litoria caerulea) in a zoo in Thailand (Pirarat et al., 2016).

Summary: Anurans

Biological or behavioural needs which are difficult to provide in captivity.

• Enrichment for amphibians should include plants and shelter, but the behavioural assessment of welfare requires more attention to understand where normal behaviour is suppressed, or abnormal behaviour is expressed.

More information is needed to understand the welfare of this animal.

• Batrachochytrium fungi are a threat to wild and pet amphibians.
• There is an absence of scientific literature relating to the reviewed species of frogs and toads in captivity in Scotland. Most studies relate to laboratory conditions.
• The species’ requirements for UVB should be established before sufficient information is available to allow responsible pet ownership, otherwise it is possible that anurans are routinely suffering from metabolic disease.

Key resources

The importance of enrichment for advancing amphibian welfare and conservation goals: A review of a neglected topic (Michaels et al., 2014).

Impacts of UVB provision and dietary calcium content on serum vitamin D-3, growth rates, skeletal structure and coloration in captive Oriental fire-bellied toads (Bombina orientalis) (Michaels et al., 2015).

6.0. Invertebrates

6.1. Cephalopods

The category “cephalopods” includes around 700 living species (Sykes et al., 2017). In Scotland, the main use of cephalopods is for food, which are wild-caught from the northeast Atlantic. Cephalopod culture (captive breeding) is not undertaken around Scotland (Pierce et al., 2010). Publications in cephalopod welfare in captivity are a result of recent concern about the experience of invertebrates in research (Horvath et al., 2013), including the COST Action CephsInAction (FA1301—http://www.cephsinaction.org/) and Cooke et al. (2019). The recognition of cephalopod cognitive abilities and their appreciation by the public for impressive demonstrations of cognitive ability has spurred interest in the suitability of captive environments to fulfil their welfare needs (Mather, 2022).

No cephalopods have been used in animal experiments in the UK in recent years (Speaking of Research, 2020), but since cephalopods kept as pets may be sourced from a similar route as those used in research, information on the welfare of cephalopods in breeding and trade are included here.

a) Breeding

Commercially breeding cephalopods is limited due to high mortality, including massive mortality events of juveniles (Morales et al., 2017), which are linked to difficulties in providing adequate nutrition (Navarro et al., 2014).

b) Housing requirements

Several recent reviews explain the health and welfare implications of keeping cephalopods (Jerez-Cepa and Ruiz-Jarabo, 2021) for research and aquaculture (Chancellor et al., 2020). There is a focus on European cuttlefish (Sepia officinalis) and the use of cephalopods in research (Fiorito et al., 2015). Husbandry procedures must take into account the fragile nature of cephalopod skin, which is easy to injure, and secondary infections can be fatal. Evidence for traumatic injury, as a consequence of hitting tank walls or fighting, and their mitigation (including softer tank walls, altering sex ratios and decreasing stocking density to reduce aggression) are described in Sykes et al. (2019). Noise levels in the laboratory setting can cause acoustic damage (damaged hair cells) in cuttlefish (Sole et al., 2017), and the levels identified as potentially harmful (low frequency sounds up to 400Hz) may inform husbandry in the domestic setting, such as the placement of aquaria near to white goods.

The concept of stress in cephalopods is not new and the National Resource Center for Cephalopods (USA) published guidance (Oestmann et al., 1997) outlining water quality parameters for cuttlefish (Sepia officinalis) and squid (Sepioteuthis lessoniana) bred for experimental use, particularly with the aim of keeping healthy populations despite the need for transport. The report includes guidance on housing and handling, identification, common health conditions and their treatments, feeding and the appropriate stocking density to avoid aggression. The use of intramuscular injections should be avoided when antibiotics can be administered in food. Beyond aggression, behavioural signs of illness, such as “changes in chromatophore display patterns or in orientation to other animals in the tank”, may require careful observation by people familiar with the species and individuals. Minimally invasive sampling from the skin surface is an alternative means of assessing stress.

Since no evidence of conditions for pet cephalopods in Scotland was found, an evaluation of the adequacy of water quality in the domestic setting is not known. However, guidelines developed for laboratory animals are available to owners; optimum water quality is defined in Fiorito et al. (2015) and recommendations for seawater filtering systems are available (Hanlon et al., 1991). The effect of copper concentration or contamination on health and welfare needs more research (Sykes et al., 2019).

c) Nutrition

The lack of a defined processed diet is identified as a limitation in the successful husbandry of cephalopods (Oestmann et al., 1997). On a simple level, cephalopods’ requirement for protein is high (for Octopus maya, nutritional requirements are 80-86% protein, (García-Garrido et al., 2013), requiring live prey from the time they use up larval yolk supplies (Fuentes and Iglesias, 2001; Morales et al., 2017). Octopus larvae require closely balanced amino acids and balanced fatty acid profiles (Navarro et al., 2014). Octopus vulgaris has a low ability to digest neutral lipids, which are found in high quantities in sardines, Family Clupeidae (Quintana et al., 2015). Octopus paralarvae fed with Artemia enriched with marine phospholipids had better growth at 12 days and survival at 28 days compared with those fed Artemia enriched with phytoplankton (Morales et al., 2017).

The Caribbean octopus, O. americanus, is easier to feed, because it will accept thawed food (Bastos et al., 2021). High-temperature processing of food makes it less digestible and specialist processing (lyophilisation) and the development of pelleted diets for commercially farmed cephalopods is still under development (Bastos et al., 2021). Live feeding of “feeder fish” have the disadvantages of creating large quantities of waste material, which needs to be cleaned out of the tank, is inefficient, toxic metals (copper) can be introduced, and there are ethical concerns around the welfare of the fish and decapods being used as food. However, frozen prey may be more effective sources of environmental enrichment than pelleted food.

Malnutrition or under-feeding during rearing can weaken cuttlefish cuttlebones and leave them susceptible to fracture. More research on appropriate nutrition for juveniles, especially calcium and magnesium deposition, would elucidate the role early nutrition plays in the development of fractures (Sykes et al., 2017) .

d) Health and disease

The development of appropriate anaesthetics for cephalopods is a recent (but see (Culloty and Mulvahy, 1992) focus of research, particularly in relation to surgical procedures carried out on experimental animals (Goncalves et al., 2012; Polese et al., 2014; Lopes et al., 2017; Escanez et al., 2018; Wellehan et al., 2020).

Summary: Cephalopods

Biological or behavioural needs which are difficult to provide in captivity.

• Feeding cephalopods is challenging due to their high requirement for appropriate protein, and live feeding live poses issues for the welfare of feeder fish and decapods, and for water quality.

Evidence of harm associated with captivity.

• Farmed and laboratory cephalopods face many challenges to their welfare; they are vulnerable to stress and injury in captive conditions.

More information is needed to understand the welfare of this animal.

• More research is needed into whether the social and behavioural needs of pet cephalopods are being met.

Key resources

Invertebrate welfare: an overlooked issue (Horvath et al., 2013)

Aquarium Maintenance Related Diseases (Sykes et al., 2019)

6.2. Decapods

The importance of decapod welfare is a current issue in animal welfare and veterinary medicine, and the legislation to establish the UK Animal Sentience Committee recognised sentience in cephalopods and decapod crustaceans Animal Welfare (Sentience) Bill [HL] - Parliamentary Bills - UK Parliament (BVA, 2021). However, their ownership as pets is not evident in published literature. Although live decapods (such as shrimps, crabs and lobsters) can be sold over the internet in the UK (Source: Crustacean Compassion), these are largely intended for cooking rather than pets.

The WoS search results included evidence on some basic principles of decapod welfare in relation to crustaceans traded for meat (Fossati, 2019), which are briefly described here.

a) Capture

Factors contributing towards mortality in capture (becoming tangled in fishing nets) were analysed in a case study at a Hawaiian Kona crab, Ranina ranina, fishery (Wiley et al., 2020). After injury, crabs were transported to a laboratory to assess the consequential level of mortality. An entire limb being pulled off (due to getting trapped in a net), increased mortality almost eight-fold compared with a limb being cut cleanly off. Crabs taken out of the water and exposed to direct sunlight for two hours had a 16.7% risk of mortality.

b) Transport and handling

Lorenzon et al. (2008) measured a panel of potential biomarkers, which could indicate harmful physiological effects of transport: “glucose, lactate, total protein cholesterol, triglycerides, chloride and calcium concentrations, pH, haemolymph density, and total haemocyte count (THC)”.  Transport in air was found to be less disturbing than transport in water, and lactate concentrations remained high in both treatments, suggesting exertion and energy depletion.

The welfare of decapod crustaceans in transport involves a number of physiological processes, which must adapt to artificial conditions, causing weakened ability to deal with disease challenges, and failure to cope with acute stressors may increase mortality. These factors, explained in detail in Lorenzon (2008), are briefly:

• Starvation prior to transport, leading to depletion of energy stores (including protein catabolism)
• Low oxygen and high ammonia concentrations (both exacerbated by high stocking densities)
• Emersion and air exposure, gill drying
• Temperature changes
• Handling
• Interactions with other animals
• Reduced total haematocyte concentration, leading to immunosuppression

In the green shore crab, Carcinus maenas, all of the handling techniques assessed in a laboratory study (gentle transfer in containers without physical touching, 10 minutes emersion or 10 minutes emersion with shaking (Wilson et al., 2021)), resulted in physiological stress responses. Useful indicators of transport stress were identified (oxygen consumption, haemolymph glucose and L-lactate), and these increased in proportion to the severity of the handling procedures. Oxygen consumption can remain high for 14 hours after transport, and the greatest increases are found in crabs, which are physically touched or shaken, with emersion (removal from water) being a lesser factor.

Summary: Decapods

Evidence of harm associated with captivity.

• Capture and transport are stressful to decapods and can cause severe injury. Air transport may be a less disturbing method of transport than water transport.

More information is needed to understand the welfare of this animal.

• Buying crabs as pets (e.g., hermit crabs) is evidently possible due to their listing on UK sales websites, but evidence of their welfare as pets is not published.
• “Cleaner shrimps” are also commonly purchased for aquaria but their welfare is so far overlooked.

Key resources

Crustaceans and snails as food and new challenges for ensuring ethical behavior toward invertebrates (Fossati, 2019)

Effects of handling during experimental procedures on stress indices in the green shore crab, Carcinus maenas (Wilson et al., 2021)

Stress effect of two different transport systems on the physiological profiles of the crab Cancer pagurus (Lorenzon et al. (2008)

6.3. ‘Tarantulas’, Family Theraphosidae

The EAZA Terrestrial Invertebrate TAG produces best practice guides for the Montserrat tarantula, Cyrtopholis femoralis (Garcia et al., 2021), which outlines some unknown factors about this tarantula’s normal biology (such as lifespan, diet, seasonality and clutch size). Key factors to provide in captivity are appropriate substrate for burrowing and high humidity. Veterinary care articles are available online, although original sources of evidence are not cited (Netisingha, 2019). Housing requirements include enclosures, which allow for climbing, are quiet and not too bright, and water dishes must be shallow to avoid drowning. Reichling and Gutzke (1998) describe the effect of temperature and feeding on size, and a Web of Science search did not reveal any information relating to the welfare of pet tarantulas at any stage in their life in captivity.

Summary: Tarantulas, Family Theraphosidae

Biological or behavioural needs which are difficult to provide in captivity.

• Guidance on husbandry is available to owners for the Montserrat tarantula, Cyrtopholis femoralis, which has apparently quite simple needs, but more investigation of its normal behaviour in a more complex or wild environment is warranted.

More information is needed to understand the welfare of this animal.

• No additional information on tarantulas from WoS or veterinary journals was found.

Key resources

Best Practice Guidelines for the Montserrat arantula (Cyrtopholis femoralis) (Garcia et al., 2021)

When your pet has eight legs (Netisingha, 2019).