Introduction

Nutrition is an important aspect of health and management in captive reptiles, and imbalances can lead to several common metabolic conditions such as nutritional secondary hyperparathyroidism and hepatic lipidosis (Oonincx and van Leeuwen, 2017; Divers, 2019). High fat diets are thought to be a predisposing factor to hepatic lipidosis, among other husbandry-related factors such as reduced activity and nonbreeding females (Divers and Cooper, 2000). Thus, investigating the feeding practices of captive inland bearded dragons (Pogona vitticeps), one of the most popular pet reptiles in North America (Schabacker, 2019), would be valuable to assess whether there are systematic dietary issues that could be associated with the high prevalence of husbandry-related disorders in this species.

There have been no surveys published that evaluated the feeding practices of owners of bearded dragons, and this information would be useful for breeders and veterinary health care teams. Resources such as webpages, pet stores, books, scientific literature, and veterinarians are available to pet owners and provide various suggestions on best diet practices. Investigating owners' preferred information sources would be valuable because it would help direct better efforts at owner education for bearded dragon dietary needs. Several publications between 1996 and 2003 offered feeding recommendations for bearded dragons, including the suggestion for leafy greens, vegetables, and insects (de Vosjoli and Mailloux, 1996; Donoghue and McKeown, 1999; Cannon, 2003). However, specific instructions regarding the quantity of dietary ingredients were not clear. Recommendations on frequency of feeding varied from daily to every other day (de Vosjoli and Mailloux, 1996; Donoghue and McKeown, 1999; Cannon, 2003).

Ecological studies report various gastric contents in free-range bearded dragons. One study reported adult inland bearded dragons to be almost exclusively herbivorous, with the majority of the gastric contents (90%) being plant material and a minimal amount (10%) of animal material (Macmillan et al., 1989). Another study found the gastric contents of adult inland bearded dragons to be 54.4% plant material and 41.5% animal material such as termites (Isoptera) (Oonincx et al., 2015b). Eastern bearded dragons (Pogona barbata) are reported to be omnivorous, with males consuming more plant material and gravid females tending to consume more animal material (Wotherspoon and Burgin, 2016). From these data, it was suggested that bearded dragons are opportunistic predators that mostly eat plants (forbs, woody plants, grasses, succulents) (Boyer and Scott, 2019a) when arthropods are limited and that a variety of dark leafy greens and insects in captivity would resemble the natural diet of inland bearded dragons (Oonincx et al., 2015b). However, the proportions of plant and insect material recommended for captive adult bearded dragons reported in literature vary between 50 and 90% plant material and between 10 and 50% animal material (de Vosjoli and Mailloux, 1996; Stahl, 1999). It is suspected that many pet bearded dragons are being offered diets consisting of mainly larval insects, with fewer adult insects and plant material being offered.

Establishing a properly balanced diet for a pet bearded dragon can be difficult because it requires multiple components, and pelleted diets may not be complete or readily accepted (Douglas et al., 1999; Boyer and Scott, 2019a). Also, attempting to mimic wild diets for pet bearded dragons may not be feasible or appropriate because several important factors differ between wild and captive populations. To account for the complexity of balancing captive diets and to prevent dietary deficiencies, supplements are typically recommended, with a variety of products marketed for pet reptiles. However, only a few of these supplements have been tested for efficacy in gut loading and dusting of feeder insects (Douglas et al., 1999; Finke et al., 2005). The unknown efficacy of supplements, combined with improper diets, can result in nutrient requirements not being satisfied, leading to potential deficiencies or excesses.

The objective of this study was to survey bearded dragon owners in the United States and Canada to learn more about their feeding practices and supplement use. This information can identify areas where veterinarians can promote client education and suggest potential dietary risk factors to be further studied in relation to nutrition-related disorders. In addition, the results of this survey may serve to promote the development of nutritional assessment guidelines for this species and further research in this field.

Materials and Methods

A survey titled “Nutritional Survey of Bearded Dragon Dietary Habits in North America,” with multiple choice and open text questions, was made available online (Qualtrics XM 2020, SAP Software Company, Provo, UT, USA) following research ethics board approval (REB 19-08-041) from the University of Guelph, Canada. Self-selecting primary caregivers to bearded dragons were invited to participate in the survey if they were >18 yr of age or had guardian consent and resided in Canada or the United States. The survey (Supplementary Appendix 1) had 32 questions in total and was intended to be completed once per household. It began with four questions about the pet demographics, including where the animal was acquired (e.g., pet store, breeder, rescue group) and the age and sex of the animal. Subsequently, a set of six questions collected information on the proportion of larval insects (e.g., mealworms, waxworms, superworms [Zophobas morio]), adult insects (e.g., crickets, beetles), and plant material fed to the bearded dragon. Open text questions were designed to allow the survey participant to list specific types of insects, vegetables (root, leafy greens), and fruits offered. Next, a set of thirteen questions addressed water provision, calcium and multivitamin supplementation, and ultraviolet-B light or sun exposure. The subsequent set consisted of four questions about animal health and veterinary care as well as the level and source of knowledge in husbandry. A set of four questions focused on demographics of the survey participant and a final question at the end of the survey provided an option to enter a draw for a gift card as an incentive to complete the survey. For an owner with multiple bearded dragons, the questions regarding age, sex, and acquisition of the animal were repeated. A draft version of the questionnaire was beta tested by five veterinarians to evaluate clarity of wording and ease of answering questions. The wording of the questions was also reviewed by an independent data analyst. Once corrections were made, the final survey was prepared for distribution.

The final, approved questionnaire was distributed online through veterinary professional groups and social media outlets including the Ontario Veterinary College bulletin and Facebook page, Twitter handle from the Ontario Veterinary Medical Association, e-newsletter from the Canadian Veterinary Medical Association, the American College of Zoological Medicine Facebook page, and the College of Veterinarians of Ontario e-newsletter. The announcement in these communications encouraged veterinarians to share the link with their clients and on their social media pages. Although the online survey link was accessible to respondents for a 5 month period between March 2020 and July 2020, it was only actively promoted during the first 30 day period. Survey responses were collected, collated, and assesed with descriptive statistics. Dietary practices were compared with the recommendations suggesting 50% plant material and 50% insects be offered to adult bearded dragons (de Vosjoli and Mailloux, 1996).

Results

In total, 455 survey responses were collected between March 2020 and July 2020. Entries listing the number of bearded dragons owned and no other information were removed from the data set, resulting in 405 surveys for analysis. Of the remaining entries, 346 respondents reported the complete demographics of their bearded dragons; 342 respondents answered all questions pertaining to their bearded dragons' diet, except for 15 respondents who did not specify supplement use; and 302 respondents reported their personal demographics and knowledge level. The median age of the bearded dragons (n = 346) in this study was 8 yr (range, <1–20 yr) and the mode was 1 yr (Fig. 1). Five bearded dragons were reported to be between 6 and 8 months of age. Bearded dragons in this survey mainly came from pet stores or a third party such as a shelter, rescue, or friend (Fig. 2). There were more male (53.2%; n = 184/346) than female (38.7%; n = 134/346) bearded dragons owned by survey participants. When devising a nutritional plan for their bearded dragons, the majority of owners consulted specialized herpetologic webpages and forums, whereas a smaller portion consulted their primary veterinarian or books, and a few consulted a pet store or a board-certified zoological medicine specialist (Fig. 3). Approximately 58.9% (n = 178/302) of the survey respondents considered themselves to have an intermediate level of knowledge in reptile husbandry, whereas 23.5% (n = 71/302) considered themselves to have advanced knowledge and 16.6% (n = 50/302) considered themselves to be novices.

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Owners were questioned on the proportion of food offered to their bearded dragons (Fig. 4). The most common diet consisted of 1–25% larval insects, 1–25% adult insects, and 51–75% plant material (Fig. 4). A significant portion of owners (55.3%; n = 189/342) fed >50% insects, although when analyzed separately, a majority fed no more than 25% larval insects (57.6%; n = 197/342) and no more than 25% adult insects (69.6%; n = 238/342). In addition, 47.4% (n = 162/342) of responders were feeding <50% plant material. The most common feeder insects offered to the pet bearded dragons included a combination of larval superworms (73.9%; n = 253/342) and hornworms (Manduca sexta) (67.8%; n = 232/342) (Fig. 5) and adult house crickets (Acheta domesticus) (74.6%; n = 255/342) (Fig. 6). Of the plant items offered by owners, berries were the most common, followed by lettuce and carrots (Fig. 7). However, when evaluating the proportions of plant items offered, many owners offered larger portions of leafy greens (69.6%; n = 238/342) and smaller portions of vegetables (45%; n = 154/342). Fruits were offered by 70.5% (n = 241/342) of owners, although generally offered in small portions (<25%) by a majority of owners (92.1%; n = 315/342). Only 64.6% (n = 221/342) of survey respondents always had water available in a bowl for their bearded dragons.

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Younger bearded dragon owners (those identifying as <18 yr of age with guardian consent) predominantly fed diets rich in larval insects. By comparison, respondents in other age groups fed a diet low in larval insects (Fig. 8). Most owners >18 yr of age fed their bearded dragons a smaller proportion of insects and a larger proportion of plant material (Fig. 8).

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A majority of owners dusted insects with calcium before feeding, every other day or on a weekly basis, and tended to use a calcium powder that contained vitamin D₃ (Fig. 9). Fewer owners dusted insects with multivitamins, and those that did predominantly dusted on a weekly basis (37%; n = 121/327) (Fig. 9). In addition, a large portion (70.6%; n = 231/327) of owners also gut loaded the insects (Fig. 9). Fewer owners dusted plant material with calcium powder (48.9%; n = 160/327) or a multivitamin powder (32.1%; n = 105/327). A large number of respondents (92.4%; n = 302/327) provided ultraviolet B (UVB) radiation for their bearded dragons. A subset of these owners (57.8%; n = 189/327) took their bearded dragons outside for natural UVB exposure.

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Discussion

This survey represented the diet and supplements offered to adult male and female bearded dragons in Canada and the United States. All bearded dragons from this survey were included in the adult group, although sexual maturity is reported to be at 18–24 months (Raiti, 2012). References that discuss diet for juveniles refer to animals <5 g (Macmillan et al., 1989) or <4 months (de Vosjoli and Mailloux, 1996). In addition, one subadult was reported and included in the ecological study by Oonincx et al. (2015b). A slightly higher prevalence of male bearded dragons was present in this data set, but sex of the animal was considered unlikely to influence the type of diet offered. When devising a dietary plan, the majority of owners consulted herpetologic webpages and forums instead of books and veterinarians. This choice was likely due to the ease of access to internet webpages and the absence of cost. These webpages and forums generally discuss people's experiences and advice in captive care of their pet bearded dragons.

When analyzing the distribution of plant material, adult insects, and larval insects, it is apparent that approximately one half of the responders were feeding >50% greens, 1–25% larval insects, and 1–25% adult insects. Compared with some recommendations for adult bearded dragons of 50% plant material and 50% insects (de Vosjoli and Mailloux, 1996), similar results were highlighted, with approximately one half (55.3%) of respondents reportedly feeding too many larval and adult insects and approximatly one half (47.4%) of respondents feeding not enough leafy greens. This disparity was even more obvious when compared with the recommendations of 90% plant material and 10% insects in other references (e.g., Stahl, 1999). When these data were evaluated based on age of the respondent, owners younger than 18 yr of age were more likely to offer too many insects, mainly larval insects, and not enough plant material. The proportion of inadequate diets offered is reflected in the fact that 75.5% of respondents considered themselves to have a low-to-intermediate level of knowledge of bearded dragon husbandry. This may be due to a lack of access to scientific literature or owners not engaged with the care of their pets. Because larval insects are high in fat (Barker et al., 1998), it is plausible that an increased intake of larval insects could be one underlying risk factor promoting obesity and hepatic lipidosis in this lizard species. Larval insects tend to be higher in palmitic acid (saturated fatty acid) than adult insects, which contain more linoleic acid (polyunsaturated fatty acid) (Finke, 2002, 2015b). Diets high in saturated fatty acids have been linked to metabolic and cardiovascular disease in rats and humans (Oliveira Junior et al., 2013; Briggs et al., 2017). Palmitic acid, in particular, has been linked to dyslipidemia, hyperglycemia, increased fat accumulation, and increased inflammation in humans with excessive carbohydrate and caloric energy intake along with a sedentary lifestyle (Carta et al., 2017).

Superworms (17.7% as fed respective 42.0% crude fat dry matter [DM]) and hornworms (20.7% as fed respective 21.7% crude fat DM) were the most common larval insects offered, and superworms have been shown to contain some of the highest percentages of fat compared with other larval insects (Landry et al., 1986; Finke, 2002). House cricket (6.8% as is converted to 22.1% crude fat DM) was the most common nonlarval insect offered and has been shown to contain significantly less crude fat than the larval superworm but comparable amounts of fat to the hornworm on a DM basis (Finke, 2002). Of all the insects offered, silk worms (Bombyx mori) (1.4% as is converted to 8.0% crude fat DM) have the highest levels of retinol and the lowest percentage of fat (Finke, 2002). By contrast, of the offered insects, black soldier fly (Hermatia illucens) larvae have the best calcium-to-phosphorus ratio, independent of bioavailability (Finke, 2013). This assessment of crude fat suggests that although the most common larval insect offered has a high fat content, a combination of adult and low fat larval insects would be ideal. Insects from the wild are nutritionally different from commercially raised insects and have lower fat with higher carotenoids, vitamin E, and omega-three fatty acids (Finke, 2015a; Oonincx et al., 2015a; van Broekhoven et al., 2015), which may be due to diet and energy expenditure (Finke and Oonincx, 2014, 2017). Nutritional composition differences between wild and commercial insects may play a significant role in fat metabolism and storage in bearded dragons, especially when offered in abundance year-round. In addition, wild-caught insects have a higher concentration of vitamin D than commercial insects, and provision of UVB to insects has been proven to increase their vitamin D₃ levels (Finke, 2015b; Oonincx et al., 2018). However, raising commercial insects with the provision of UVB is not standard, and making this information readily available to pet stores may improve the nutritional quality of feeder insects.

Berries and carrots, two commonly offered plant materials to pet bearded dragons in this study, contain high amounts of simple carbohydrates that can be converted into fat when fed in excess and can lead to obesity and metabolic disorders. Carbohydrates have also been linked to hepatic lipidosis in humans (Basaranogul et al., 2015). Although fruits were offered to more than one half the bearded dragons included in this survey, with berries being the most common overall, they made up <25% of the offered plant material for the majority of these animals, which consisted mostly of leafy greens with a few vegetables. Current literature does not recommend fruits in the diet; some researchers found fruit to be a significant risk factor for dental disease in inland bearded dragons (Boyer and Scott, 2019a; Mott et al., 2021). Studies following free-roaming bearded dragons over several seasons, over time, and in different habitats are required to gain a better understanding of their natural diet and to make better recommendations for a captive diet. A variety of leafy greens and a limited amount of vegetables, flowers, and insects have been suggested (Cannon, 2003; Boyer and Scott, 2019a). However, the composition of vegetation in the wild is different from commercially available vegetables, which are low in minerals and fiber and high in simple carbohydrates (Macmillan et al., 1989; Allen and Oftedal, 2003; Raiti, 2012; Boyer and Scott, 2019b). The differences between wild and commercial vegetation raise questions about whether store-bought produce accurately represents plant matter eaten in the wild. It should also be noted that many other nonnutritional risk factors may be implicated in the pathophysiology of hepatic lipidosis in this species (Divers, 2019; Divers and Cooper, 2000).

Because of the inverse calcium-to-phosphorus ratio of some plant material and most commercially raised insects (Finke, 2015a), dusting and gut-loading recommendations have also been made. Recommendations vary from dusting insects and plant material daily with calcium powder to dusting once or twice if fed several times in a week (Donoghue and McKeown, 1999; Raiti, 2012; Finke and Oonincx, 2017). However, because calcium salt is better absorbed with food and inhibits phosphorus absorption (Boyer and Scott, 2019a), it likely should be used every time food is offered to improve the calcium-to-phosphorus ratio. Results from this survey suggest that dusting insects with calcium powder is a common practice, although calcium dusting of plant material is less common. The majority of owners provided calcium with vitamin D₃, a finding that is consistent with the literature (Raiti, 2012; Boyer and Scott, 2019a). This recommendation is not evidence based for bearded dragons because the only study completed thus far on this topic indicated that oral supplementation of vitamin D₃ was ineffective at increasing plasma calcidiol and calcitriol concentrations compared with ≥2 h of UVB exposure (Oonincx et al., 2010). These diurnal animals should be able to synthetize their own endogenous vitamin D₃ through sufficient UVB, and almost all survey respondents provided UVB for their bearded dragons. Currently, guidelines for calcium supplementation in bearded dragons remain vague. Nutritional deficiencies leading to metabolic bone disease can occur with insufficient dietary calcium, whereas dystrophic mineralization can be induced with oversupplementation, as demonstrated in the leopard tortoise (Geochelone pardalis) (Fledelius et al., 2005). Specific data for guidelines in bearded dragons are lacking.

Many respondents reported that they gut loaded insects offered to their pet (Supplementary Appendix 1, question 15). However, owners were not questioned on types of gut-loading diets provided to these insects, thereby limiting the value of this question because they could have simply been feeding the insects. In addition, a typo in the survey was made asking if gut loading was provided for 8 h instead of 24–48 h. Gut loading insects for 24–48 h with an 8% calcium diet has been recommended to improve the calcium-to-phosphorus ratio (Zwart and Rulkens, 1979; Strzelewicz et al., 1985; Allen and Oftedal, 1989). Various gut-loading diets are available, but plant-based diets are more palatable to house crickets (Attard, 2013). A few of these diets have been evaluated to assess whether calcium content is adequate, and only two commercially available products have been proven efficacious in crickets and superworms (Finke et al., 2005; Latney et al., 2009). Unfortunately, these products are not readily available in Canada, making it unlikely that Canadian responders were appropriately gut loading their insects. Because numerous untested products are available, it is possible that many of the insects were not appropriately gut loaded. In addition to calcium supplementation, multivitamin supplementation is advised because feeder insects are deficient in several vitamins (Boyer and Scott, 2019a). Some authors advise weekly supplementation, whereas others recommend supplementation once to twice a month, although there are no studies to support these recommendations (Boyer and Scott, 2019a). Dusting insects and plant material with multivitamins was reportedly done by fewer respondents; the frequency was weekly rather than daily. The lack of multivitamin dusting could result in vitamin E deficiency, which plays an essential role in fat metabolism (Wong et al., 2017). Insufficient vitamin E could pose a potential risk factor for the development of hepatic lipidosis, as demonstrated in lambs (Menzies et al., 2004).

Although inland bearded dragons are desert dwelling, they do drink water and need regular access to fresh, clean water (Boyer and Scott, 2019a). A large portion of respondents did not have water avaliable in a bowl for their bearded dragons. However, this finding did not account for water not being offered in more nontraditional ways such as soaking.

Three limitations of this study are 1) possible recall bias by owners answering survey questions; 2) reporting bias in the data because owners not responding to a question were not included in the calculations of proportions; and 3) misleading or unclear wording in questions 9, 10, 14, and 15 (Supplementary Appendix 1). These owners may have left a question blank instead of selecting what they would consider a negative response, if they did not know the answer, or if they did not want to complete the survey. For example, an option for dusting with multivitamins on a less frequent basis, such as monthly (question 14), feeding a commercial pelleted diet, or feeding nymphal crickets was not offered, so a subset of respondents may have not answered questions pertaining to diet. In question 9, fruits are not listed in the proportion of plant material offered, whereas the follow-up question 10 does ask for the percentage and type of fruits offered, which could have biased the responses. The exact amount and frequency of food offered were not evaluated in this survey and might have provided important information on the total caloric intake per meal because excess caloric intake and obesity are known to be major problems in captivity (Boyer and Scott, 2019a) and could be linked to hepatic lipidosis. The data for owners that identified in the age group 60–69 yr (n = 6/302) were likely not representative, with a low number of responses in this category. The species of bearded dragon owned was not identified and assumed to be P. vitticeps because it is the most common species in the pet trade. However, other species, such as P. barbata, may have been included and are known to consume more insects and less plant material in their natural diet (Wotherspoon, 2007). Additional limitations include a selection and inclusion bias skewing the data toward more proactive owners, because the survey link was disseminated among veterinary staff and veterinary-related social media. The number of owners that feed an inadequate diet in the general population is likely much higher than reflected in this survey. A selection bias may also be represented in the number of individuals who devised a nutritional plan with their primary veterinarian. Multivariate statistics were not completed on the data, and this was also a potential limitation; however, complex statistics were considered beyond the scope of the study aim of reporting diet types and feeding management of bearded dragons.

Clear and well-researched nutritional guidelines endorsed by specialty veterinary organizations should be developed for owners and distributed at pet stores, rescue centers, and online. Educational infographics on bearded dragon health, diet, and husbandry should be promoted widely by the veterinary profession. Veterinarians who provide consultation to bearded dragon owners need to be prepared to discuss nutritional practices, supplement use, water provision, and the current evidence-based recommendations. However, large knowledge gaps about nutritional requirements for bearded dragons can make such discussion challenging. Bearded dragons have a high prevlance of hepatic lipid accumulation, and diet should be closely scrutinized as a risk factor (Barboza et al., 2022). Until further evidence-based recommendations are avaliable, owners should be urged to limit the amount of carbohydrates and fatty larval insects offered to their bearded dragons and to provide diets higher in fiber and adult or low fat larval insects. The ideal composition and quantity of plant and insect material offered (e.g., lower carbohydrate, higher fiber) and appropriate type, amount, and frequency of supplementation require further investigation.