Introduction

Pathogens (e.g., viruses, bacteria, fungi) transmitted through the wildlife trade have received increasing attention in the past 15 years due to the H1N1 (swine flu), H5N1 (bird flu), and SARS-CoV-2 (COVID-19) outbreaks [1,2]. Wildlife are targets of, and reservoirs for, pathogens that may infect native species, domestic animals, and humans. Wildlife are considered to be the source of at least 70% of all emerging diseases [3,4]. Increasing global trade in wildlife and environmental change have generated new infectious disease dynamics and pathways that allow for the rapid spread of pathogens geographically and between species, thereby threatening biodiversity and animal and public health [3–6].

In this paper we focus on pathogen transmission through the herpetological trade, which has resulted in severe ecological, economic, and human health consequences [7–9]. The fungal pathogens Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal) cause chytridiomycosis (‘chytrid’), an emerging infectious disease that is considered the leading infectious disease threat to biodiversity [7,8]. Ranaviruses (family Iridoviridae) are widespread, host-unspecific emerging dsDNA viruses that produce systemic infections in amphibians, reptiles, and fish [10,11]. Salmonella bacteria are zoonotic pathogens that cause salmonellosis and are transmitted to poultry, livestock, and humans through direct and indirect contact with herpetofauna [9,12]. Transmission of Bd, Bsal, ranaviruses and Salmonella has been exacerbated by the trade in herpetofauna [5,10,13].

Batrachochytrium dendrobatidis, Bsal and ranaviruses are main drivers of global declines in amphibian populations [7,10,14,15], which is concerning because recent estimates suggest that 41% of amphibian species are threatened globally [16]. Batrachochytrium dendrobatidis has infected >500 species from all three orders of Amphibia and has contributed to declines and extinctions of >200 amphibian species globally [10,15]. Batrachochytrium salamandrivorans has been detected across salamanders, frogs, and toads, including some of the most widely traded amphibian species [8], and has resulted in mass mortalities of native wild salamander populations [13,15]. Both Bd and Bsal are extremely difficult to eradicate once they are established in the wild [7,13].

Ranaviruses infect >175 ectothermic vertebrate species across 52 families [14] and are characterized by high infection prevalence and sudden mortality in multiple species [11]. Ranaviruses may cause severe systemic diseases in marine and freshwater fish and have negatively impacted aquaculture industries globally [14]. Ranaviruses infect species that are both economically important (e.g., the North American bullfrog Rana catesbeiana) and of conservation concern (e.g., the gopher tortoise Gopherus polyphemus) [14]. Interclass transmission of ranaviruses may occur [14]. Humans accidentally disperse ranaviruses through the transportation of contaminated water or soil (e.g., through recreational activities, agricultural grazing, and other anthropogenic disturbance [11]) and by using fishing bait infected with ranaviruses (e.g., Ambystoma tigrinum virus infection in barred tiger salamander Ambystoma mavortium larvae sold as fishing bait in the southwestern United States [14]).

Salmonella is a globally important zoonotic pathogen (typically transmitted through human consumption of Salmonella-contaminated food of animal origin), which results in $3.6 billion annually in economic costs [9]. Salmonella enterica is the second most frequently reported zoonotic pathogen in the World Organization for Animal Health (OIE) World Animal Health Information System (WAHIS)-Wild interface [3]. Salmonella may remain viable for >30 days in most microcosms and colonizes both wild and captive amphibians and reptiles [12,17,18]. The trade in amphibians and reptiles (which are natural reservoirs of Salmonella [12,17,18] has contributed to Salmonella transmission, with ≥6% of human salmonellosis cases being attributed to direct or indirect contact with reptiles [9,18,19]. Amphibians and reptiles may also contribute to environmental Salmonella contamination in agricultural and recreational areas [17]. Although infection usually causes self-limited gastroenteritis in humans, severe illness and death may occur in children, the elderly and immunocompromised adults [9,18,19]. Antimicrobial and multi-drug resistance in Salmonella strains carried by pet herpetofauna is a growing public health safety concern, and may result in increased disease severity, longer hospitalizations, and higher economic costs, leading the World Health Organization to include Salmonella on its priority list of 12 antibiotic-resistant bacteria [9,12].

The transmission of Bd, Bsal, ranaviruses and Salmonella through the live herpetological trade occurs because herpetofauna are often shipped at high densities [12,20]. Mixing of animals under dense conditions induces stress, especially in hierarchical, territorial, and aggressive animals or animals with largely solitary behaviors in the wild (e.g., Tokay geckos Gekko gecko which are imported for the pet trade [12]). Stress associated with captivity and transport results in immunosuppression, increased mutations and exchange of antibiotic resistance among enteric bacteria, increased pathogen prevalence, and increased shedding and transmission of pathogens by captive herpetofauna [12,20]. Studies show that pathogen prevalence and serotype richness in captive herpetofauna may increase in the 6 months following import [12], which suggests that disease risks may increase once animals have been distributed into the domestic trade.

Biosecurity at ports of entry is thus critical to preventing pathogen transmission through the live herpetological trade [5,21]. However, to date, poor application of biosecurity at ports of entry has resulted in rapid pathogen spread through the transport of infected animals into new regions [5,6,10,15]. Border inspections of wildlife imports are typically aimed at seizures of illegal shipments, rather than prevention of pathogen spread [5]. For example, the United States Fish and Wildlife Service (USFWS) primarily assesses the conservation status of imported animals into the United States, the Center for Disease Control (CDC) focuses on health risks associated with non-human primates, African rodents and bats, and the United States Department of Agriculture (USDA) regulates non-domestic hoofstock, birds and mammals that are imported from countries that are positive for reportable diseases [5]. Improved practices to reduce animal stress and pathogen transmission during transport, more rigorous screening of herpetofauna imports for pathogens, and quarantine of imported animals are needed to prevent pathogen pollution through the introduction of novel pathogens, unique genetic strains of existing pathogens, or multi-drug and antibiotic resistant pathogens into new regions [12,20,21]. Once captive herpetofauna are released into the domestic trade it is extremely difficult or impossible for government agencies to prevent pathogen transmission to native wildlife, domestic animals, or humans, owing to jurisdictional boundaries across government agencies and insufficient funding and staff to actively monitor and regulate trade [12,21].

Unfortunately, implementation of biosecurity measures at ports of entry is often highly political, owing to the economic importance of trade and the substantial costs to the state of biosecurity [22,23]. Investment in effective biosecurity relies on an educated public, legislature and business community that recognizes the risks of pathogen transmission through the herpetological trade and is willing to financially and politically support biosecurity [24–26]. However, social sciences research on public support for biosecurity measures to prevent pathogen transmission through the herpetological trade is missing from the literature–a critical gap given the size of the global trade in herpetofauna [3,6]. Our study was designed to help address this research gap. We conducted research in the United States to test how the public’s values, risk perceptions, knowledge of disease transmission, trust in government, and demographic characteristics influenced their support for biosecurity measures to prevent pathogen transmission through imports of live herpetofauna.

Existing research shows that the public’s support for actions to mitigate risks depends on their risk perceptions [25,27]. Although actual risk depends on the true consequences of a hazard and the objective probability of a negative outcome, risk perceptions are subjective judgments that vary across individuals and influence their behavior under uncertainty [24,28,29]. Risk perceptions are commonly measured in terms of severity and susceptibility (perceived likelihood of occurrence) [24,30]. People’s risk perceptions depend on the specific hazards being evaluated (e.g., pathogen transmission associated with the herpetological trade), their familiarity with or knowledge of these risks, their risk sensitivity (i.e., the weight that they place on risk), their attitudes towards the agents generating risk (e.g., the herpetological trade), and their moral concerns about human interference with nature [24,27,28,30,31]. Women and older individuals tend to have higher risk perceptions related to pathogen transmission through the wildlife trade, whereas individuals with children under the age of 18 or a university degree have lower risk perceptions [24]. Prior research suggests that higher risk perceptions associated with pathogen transmission increase support for biosecurity [24,32].

Research also suggests that public support for biosecurity depends on the public’s trust in the government to mitigate disease risks (referred to as social trust) [6,27,29,30,32–35]. Social trust encompasses the public’s willingness to rely on decision-makers and agency staff who are responsible for biosecurity. Social trust plays an important role in public support for government actions when the public lacks the knowledge, ability, or resources to make independent decisions or identify appropriate actions to mitigate risks such as pathogen transmission through the import of herpetofauna [33,36]. The public is likely to express higher levels of social trust if they evaluate agencies’ past performance in managing risk (i.e., perceived competence or ability) positively and if the agency shares their understanding of a problem, the options available to address the problem, and the relative effectiveness of each of these options [29,30,32,33,35,37].

People’s support for improved biosecurity at ports of entry likely also depends on their values. We focus on four core values which underpin people’s behavior: biospheric, altruistic, egoistic, and hedonic values [38–40]. Biospheric values pertain to people’s concern for the environment, altruistic values encompass their concern for other people’s welfare and wellbeing, egoistic values focus on concern for personal resources, power and achievement, and hedonic values relate to pleasure, comfort, and reduced effort [39]. The relative weights that people place on each of these four values influence their environmental self-identity, personal norms, and risk perceptions [31], which in turn determine their behavior [39,40]. Individuals with strong biospheric and altruistic values (self-transcendence values) are more likely to support pro-environmental interventions because they are concerned about conservation and/or how improved environmental quality supports the health and wellbeing of current and future generations [31,39,40]. By contrast, individuals with strong egoistic and hedonic values (self-enhancement values) are less likely to support interventions that require behavior change and funding, which may be uncomfortable or costly to the individual [38–40]. Thus, we would expect that people with strong biospheric or altruistic values would be more likely to support improved biosecurity, whereas individuals with strong egoistic or hedonic values would be less likely to support these interventions.

However, messaging may be used to highlight disease-related risks that would resonate with individuals who have strong egoistic or hedonic values, such as economic costs or loss of recreational activities associated with pathogen transmission. Health concerns related to pathogen transmission suggest that the public may also be responsive to One Health messages and justification for improved biosecurity [24]. One Health emphasizes that human and animal health are interdependent and fundamentally linked to ecosystem health [3]. If the general public perceives that pathogen transmission is exacerbated by human activities (e.g., the trade in herpetofauna) then their support for biosecurity measures is likely to be higher [30]. However, if the general public perceives diseases to be ‘natural’ (i.e., a natural phenomenon) then their support for biosecurity is likely to be lower [30].

Based on the existing literature, we predicted that the public’s support for improved welfare of herpetofauna during transport and enhanced biosecurity at ports of entry would be positively correlated with risk perceptions (including prior familiarity with or knowledge of pathogens transmitted by herpetofauna, risk sensitivity, and moral concerns about human interference with nature), perceptions that pathogen transmission is exacerbated by human activities, social trust, and biospheric or altruistic values. We further predicted that the public’s support for improved biosecurity would be negatively correlated with egoistic or hedonic values, or the perception that diseases are a natural phenomenon. Finally, we predicted that demographics and different risks associated with pathogen transmission (ecological, economic, human welfare) would influence public support for biosecurity measures. See Fig 1 for our conceptual framework of how different risks associated with the live herpetological trade and the general public’s values, attitudes, risk perceptions and demographics would influence their support for biosecurity.

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Fig 1. Conceptual model of how respondents’ socio-psychological and demographic characteristics may influence their support for biosecurity measures to prevent the transmission of pathogens into the United States through the importation of herpetofauna.

https://doi.org/10.1371/journal.pone.0262719.g001

Methods

Results

We collected a total of 2,007 completed surveys (498 from California, 498 from Florida, 507 from New York, 504 from Texas). A total of 1,054 respondents (52.5%) were female (range of 50.2% for Texas to 55.2% for New York; S1 Table). The median age range for respondents was 45–54 years (median of 45–54 years for California, Florida, and New York; median of 35–44 years for Texas; S1 Table). The median education level for respondents was some college or an associate or technical degree for respondents from each state (S1 Table). A total of 1,585 respondents (79.0%) described themselves as white (range of 69.7% for California to 85.1% for Florida) and 463 respondents (23.1%) stated that they were Hispanic and/or Latino (range of 14.8% for New York to 37.5% for Texas; S1 Table). On average, respondents described their political views as moderate (4.12±1.60 where extremely liberal = 1, moderate = 4, and extremely conservative = 7; 3.86±1.65 for California; 4.33±1.59 for Florida; 3.88±1.54 for New York; 4.40±1.54 for Texas). In total, 607 respondents (30.2%) stated that their household contains members <18 years old (range of 27.1% for Florida to 37.5% for Texas; S1 Table). Most respondents (n = 1,338, 66.7%) owned pets, primarily dogs and/or cats (S1 Table). Only a small share of respondents owned fish (n = 142, 7.1%), reptiles (n = 64, 3.2%), or amphibians (n = 10, 0.5%; S1 Table). Similarly, only a small share of respondents owned livestock (n = 43, 2.1%), poultry (n = 39, 1.9%), or both livestock and poultry (n = 47, 2.3%; S1 Table).

Support for biosecurity measures

Most respondents strongly supported a law that requires the quarantine and veterinary observation of all imported herpetofauna (n = 1,120, 55.8%), mandatory tests of all shipments of herpetofauna for diseases of concern (n = 1,293, 64.4%), and a mandatory ‘Best Practices Program’ to improve the care and reduce the stress of transported animals and decontaminate all shipping materials (n = 1,399, 69.7%; Table 1). Cronbach’s alpha (0.828–0.852 depending on the survey version) confirmed that the items used to measure respondents’ support for biosecurity measures represented a single scale (standardized coefficients>0.7, p<0.001; S2 Table).

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Table 1. Respondents’ support for management actions to mitigate the disease transmission risks associated with the live herpetological trade (n = 2,007).

https://doi.org/10.1371/journal.pone.0262719.t001

Structural equation models

The ecological (model 1; Fig 2), economic (model 2; Fig 3), and human health and wellbeing (model 3; Fig 4) SEMs all met the criteria for good model fit. However, the best fit model that included all hazards associated with pathogen transmission (model 4; Fig 5) did not meet the criteria of CFI≥0.90. Nonetheless, we present insights from model 4 because RMSEA = 0.055 (0.053:0.056) and the estimated coefficients made sense, i.e., two of the three model fit criteria were met. We focus on the structural regression component of the SEMs below, although the complete model specifications that include the measurement models are provided in the supporting information (S28–S31 Tables).

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Fig 2. Structural equation model of direct and indirect determinants of respondents’ support for improved biosecurity measures when presented with the ecological risks associated with pathogen transmission through the live herpetological trade (model 1; n = 507).

Solid lines indicate positive correlations. Dashed lines indicate negative correlations. Line weight indicates strength of correlation.

https://doi.org/10.1371/journal.pone.0262719.g002

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Fig 3. Structural equation model of direct and indirect determinants of respondents’ support for improved biosecurity measures when presented with the economic risks associated with pathogen transmission through the live herpetological trade (model 2; n = 507).

Solid lines indicate positive correlations. Dashed lines indicate negative correlations. Line weight indicates strength of correlation.

https://doi.org/10.1371/journal.pone.0262719.g003

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Fig 4. Structural equation model of direct and indirect determinants of respondents’ support for improved biosecurity measures when presented with the human health and wellbeing risks associated with pathogen transmission through the live herpetological trade (model 3; n = 502).

Solid lines indicate positive correlations. Dashed lines indicate negative correlations. Line weight indicates strength of correlation.

https://doi.org/10.1371/journal.pone.0262719.g004

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Fig 5. Structural equation model of direct and indirect determinants of respondents’ support for improved biosecurity measures when presented with the ecological, economic, and human health and wellbeing risks associated with pathogen transmission through the live herpetological trade (model 4; n = 498).

Solid lines indicate positive correlations. Dashed lines indicate negative correlations. Line weight indicates strength of correlation.

https://doi.org/10.1371/journal.pone.0262719.g005

Consistent with our prior predictions, respondents’ support for biosecurity measures was positively correlated with their risk sensitivity. Respondents with higher sensitivity to ecological risks (β = 0.330, p<0.001, model 1; Fig 2), economic risks (β = 0.234, p<0.001, model 2; Fig 3) and human health and wellbeing risks (β = 0.226, p<0.001, model 3; Fig 4) associated with pathogen transmission through the herpetological trade were more likely to support biosecurity measures. When all three types of risks were presented to respondents, their support for biosecurity measures was directly positively correlated with their sensitivity to human health and wellbeing risks (β = 0.366, p<0.001, model 4; Fig 5), and indirectly positively correlated with their sensitivity to ecological and economic risks. Model 4 suggested that respondents with higher sensitivity to ecological (β = 0.243, p<0.001) or economic risks (β = 0.387, p<0.001) also had higher sensitivity to human health and wellbeing risks associated with pathogen transmission.

In turn, respondents’ sensitivity to risks was positively correlated with their perceived susceptibility to risks. Respondents who were more concerned about the loss of biodiversity owing to herpetological pathogen transmission had higher sensitivity to ecological risks (β = 0.418, p<0.001, model 1; β = 0.682, p<0.001, model 4). Respondents with higher perceived susceptibility to economic risks had higher sensitivity to economic risks (β = 0.915, p<0.001, model 2; β = 0.970, p<0.001, model 4). Similarly, respondents with higher perceived susceptibility to human health and wellbeing risks had higher sensitivity to these risks. Respondents who expressed greater concern about an increase in insect pests (β = 0.257, p<0.001, model 4) and insect-borne diseases owing to herpetological pathogen transmission were more likely to be sensitive to human health and wellbeing risks (β = 0.268, p<0.001, model 3; β = 0.230, p<0.001, model 4).

Respondents with higher perceived susceptibility to herpetological pathogen transmission were more sensitive to ecological risks (β = 0.400, p<0.001, model 1) and human health and wellbeing risks (β = 0.352, p<0.001, model 3; β = 0.096, p = 0.024, model 4). We also found a direct positive correlation between respondents’ perceived susceptibility to herpetological pathogen transmission and their support for biosecurity for the SEM model that focused on economic risks (β = 0.138, p = 0.026, model 2). However, respondents who believed that captive herpetofauna in the live wildlife trade are healthy were less likely to perceive susceptibility to herpetological pathogen transmission (β = -0.126, p<0.001, model 1; β = -0.291, p<0.001, model 2). We found some evidence that respondents with prior knowledge of salmonellosis were more likely to perceive susceptibility to herpetological pathogen transmission (β = 0.098, p = 0.016, model 1).

Respondents with prior knowledge of the number of live herpetofauna imported into the United States (β = 0.134, p = 0.002, model 3) and prior knowledge of herpetological imports (β = 0.107, p = 0.036, model 4) were more sensitive to herpetological trade risks, which in turn increased their sensitivity to human health and wellbeing risks (β = 0.430, p<0.001, model 3; β = 0.243, p<0.001, model 4). Our results further suggested that respondents with greater sensitivity to herpetological trade risks had greater sensitivity to the ecological risks associated with herpetological pathogen transmission (β = 0.180, p<0.001, model 1). Women (β = 0.086, p = 0.042, model 3; β = 0.151, p = 0.001, model 4) and Hispanic and/or Latino respondents (β = 0.112, p = 0.005, model 1) demonstrated greater sensitivity to herpetological trade risks, whereas respondents with more years of education demonstrated lower sensitivity (β = -0.140, p = 0.001, model 3).

Women also demonstrated greater sensitivity to general health risks (β = 0.161, p<0.001, model 2). Respondents’ sensitivity to general health risks was positively correlated with their support for biosecurity measures (positive correlation with economic risks for model 2: β = 0.126, p<0.001; direct positive correlation with support for biosecurity for model 4: β = 0.164, p = 0.002). Similarly, respondents who placed importance on protecting the health of humans demonstrated greater support for biosecurity (β = 0.108, p = 0.020, model 1; β = 0.116, p = 0.013, model 4). Respondents who agreed that disease prevalence has been made worse by humans and their activities (moral concerns) were more likely to support biosecurity measures (direct positive correlation with support for model 3: β = 0.098, p = 0.025; positive correlation with sensitivity to general health risks for model 4: β = 0.130, p = 0.012).

Respondents who liked herpetofauna were more sensitive to ecological risks associated with herpetological pathogen transmission (β = 0.139, p<0.001, model 1). By contrast, these individuals were less sensitive to human health and wellbeing risks associated with herpetological pathogen transmission when taking all possible risks associated with pathogen transmission into account (β = -0.104, p = 0.001, model 4). We found a positive correlation between whether respondents liked fish and their perceptions of susceptibility to herpetological pathogen transmission (β = 0.164, p = 0.008 for saltwater fish in model 1; β = 0.168, p = 0.046 for freshwater fish in model 2), their sensitivity to ecological risks (β = 0.117, p = 0.013 for freshwater fish in model 4), and their sensitivity to human health and wellbeing risks (β = 0.088, p = 0.032 for freshwater fish in model 3).

We found no evidence that social trust influenced support for biosecurity (p>0.05 across models). However, respondents’ values were important determinants of their support for biosecurity measures. Respondents with biospheric values demonstrated greater sensitivity to ecological risks (β = 0.166, p<0.001, model 1; β = 0.201, p<0.001, model 4), herpetological trade risks (β = 0.364, p<0.001, model 1; β = 0.425, p<0.001, model 3; β = 0.481, p<0.001, model 4) and general health risks (β = 0.605, p<0.001, model 2). We also found a direct positive correlation between biospheric values and respondents’ support for biosecurity measures for the economic risks SEM (β = 0.258, p<0.001, model 2). Similarly, we found a direct positive correlation between altruistic values and support for biosecurity measures for two of the models (β = 0.258, p<0.001, model 1; β = 0.315, p<0.001, model 3). Respondents with strong altruistic values were also more sensitive to general health risks (β = 0.505, p<0.001, model 4). We found a direct negative correlation between egoistic values and support for biosecurity measures for the SEM models that stressed the ecological and human health and wellbeing hazards associated with pathogen transmission (β = -0.182, p = 0.007, model 1; β = -0.148, p = 0.001, model 3). However, respondents with egoistic values were more likely to be sensitive to economic risks (β = 0.064, p = 0.014, model 2) and to perceive susceptibility to economic risks associated with herpetological pathogen transmission (β = 0.174, p<0.001, model 4). Respondents with egoistic values also demonstrated greater sensitivity to human health and wellbeing risks (β = 0.066, p = 0.038, model 3) and herpetological trade risks (β = 0.097, p = 0.037, model 3), thereby indirectly increasing their support for biosecurity. Finally, we found some evidence that respondents with strong hedonic values were less likely to be sensitive to ecological risks (β = -0.082, p = 0.022, model 1) but more likely to be sensitive to economic risks associated with herpetological pathogen transmission (β = 0.093, p = 0.001, model 4) and to perceive susceptibility to this pathogen transmission (β = 0.141, p = 0.001, model 4).

Discussion

Securing public support for biosecurity measures depends on a clear understanding of the public’s opinions, values, and goals, in order to increase public trust in these measures and the need for their implementation [35]. We found strong support for increased quarantine and veterinary observation, mandatory tests for diseases of concern, and best practices to reduce stress and improve the care of live herpetofauna, in order to reduce pathogen transmission through the herpetological trade. In contrast to previous studies [6,27,29,30,32,34], we found no evidence that respondents’ support for biosecurity depended on their trust in government, or their age, children under the age of 18, ownership of pets or domestic animals, engagement in recreational activities (e.g., fishing), and exposure to the live herpetological trade (consumption of frog legs, use of salamanders as fishing bait, or acquaintance with an individual who owns herpetofauna). We found some, albeit limited, evidence that women and Hispanic or Latino members of the public were more sensitive to risks associated with the live herpetological trade, whereas more educated individuals were less sensitive to these risks [24]. Rather, respondents’ risk perceptions and values played a key role in determining their support for biosecurity, which is consistent with previous findings that the public’s attitudes, beliefs, and risk perceptions are stronger determinants of their support for managing invasion risks associated with the live animal trade than their demographic characteristics [53,54]. Our finding that respondents’ socio-psychological characteristics were key determinants of their support for biosecurity has important implications for communications and messaging about biosecurity.

Respondents’ support for biosecurity strongly depended on their sensitivity to risk, which was determined by both the hazards being evaluated and their perceived susceptibility to risk [24,32]. As we predicted, individuals with strong biospheric values demonstrated greater sensitivity to ecological risks associated with pathogen transmission. These individuals also demonstrated greater sensitivity to herpetological trade risks, expressing concern about pathogen transmission from captive herpetofauna to other captive animals, native wildlife, pets, livestock, and humans. Although we did not find a direct link between respondents’ altruistic values and their sensitivity to human health and wellbeing risks associated with pathogen transmission, respondents with strong altruistic values placed importance on protecting the health of captive animals, native wildlife, the natural environment, pets, livestock, and humans. Altruistic individuals were also supportive of biosecurity when the ecological and human health and wellbeing hazards associated with the herpetological trade were highlighted. This suggests that individuals with strong self-transcendence (biospheric, altruistic) values will be receptive to One Health justifications for improved biosecurity related to the live herpetological trade, which is consistent with previous findings that these individuals tend to support interventions that improve environmental quality and secure the health and wellbeing of current and future generations [31,39,40].

Although prior studies have found weak and inconsistent relationships between self-enhancing (egoistic, hedonic) values and support for conservation measures [38,39], our findings suggest that individuals with strong egoistic values may be persuaded to support biosecurity measures for the live herpetological trade if the economic and public health risks associated with pathogen transmission are communicated. Highlighting adverse economic impacts to industries, and associated losses of revenues and employment, may resonate with egoistic individuals. We also found some evidence that egoistic individuals recognized the important role that the herpetological trade may play in transmitting pathogens and the associated negative impacts to human health and wellbeing. Egoistic individuals may be sensitive to these risks because they recognize the costs of healthcare and value their health. Although only Salmonella could be transmitted to humans, we highlighted that declines in herpetofauna populations driven by Bd, Bsal and ranaviruses could increase pest populations and transmission of insect-borne diseases. Emphasizing public health risks [55] and resilience (i.e., measures to secure communities’ economic welfare and way of life [56]) has been shown to be an effective messaging strategy to gain support for climate change interventions amongst politically conservative individuals. A similar approach may be used to tailor One Health justifications for mitigating herpetological pathogen transmission to individuals with strong self-enhancing values and those who disagree that environmental problems and pathogen transmission are exacerbated by humans (i.e., individuals who do not have moral concerns about human interference with nature and/or consider disease to be natural). However, we note other researchers’ [24,30] caution that messaging strategies pertaining to pathogen transmission by wildlife that emphasize protecting human health and economic interests may have unintended negative consequences.

Emphasizing health effects on valued wildlife species may resonate with individuals with strong self-enhancing values, as well as individuals with strong self-transcendence values, when these pathogens are not zoonotic [30]. Unfortunately, herpetofauna are typically not considered charismatic species, and members of the general public often hold negative attitudes and emotions towards these species [57,58]. It is therefore unsurprising that attitudes towards herpetofauna only appeared as a positive, indirect determinant of support for biosecurity in the model that emphasized the ecological risks associated with pathogen transmission by the herpetological trade. Respondents who liked herpetofauna (including snakes, which are often feared [57,58]) demonstrated greater sensitivity to the ecological risks associated with pathogen transmission–which is consistent with the finding that biophilia results in increased emotional connection to nature [58]. By contrast, liking for fish indirectly increased support for biosecurity across models, suggesting that people’s support for biosecurity could be attained by increasing their awareness of how pathogen transmission may adversely impact fish biodiversity [59] and economically and culturally important fisheries [60]. However, more research is needed to ascertain how attitudes towards herpetofauna and fish might influence support for biosecurity, since our measure of attitudes was restricted to asking whether respondents liked these taxa.

We found little evidence that respondents’ risk perceptions or support for biosecurity depended on their knowledge of the live herpetological trade or pathogen transmission risks associated with this trade. Nonetheless, respondents’ general lack of knowledge of the scale of the live herpetological trade, the number of industries that may contribute to the spread of pathogens, the prevalence of pathogens in the herpetological trade, the existence of Bd, Bsal and ranaviruses, and that Salmonella may be transmitted to humans by herpetofauna demonstrates that improved education and outreach on these topics is required. Imparting this information to the public may generate or reinforce intentions to support biosecurity measures. Given well-documented gaps between knowledge and behavior [61,62], we stress that information should be presented using different message framings that will resonate with members of the public who hold different values and beliefs [54,63]. Equally importantly, education and messaging should provide the public with suggested actions they can take to mitigate pathogen transmission risks. Our study focused on biosecurity actions that were unlikely to directly impact respondents in terms of cost or inconvenience, but our findings may also be used to consider how improved biosecurity behaviors by individuals may be leveraged by combining appropriate messaging with actions to make these behaviors easier to adopt (e.g., providing bait disposal containers at fishing sites [62]).

Conclusions

Trade in live herpetofauna poses serious ecological, economic, and public safety risks through the transmission of pathogens to native wildlife, domestic animals, and humans. Although improved biosecurity is required in the United States to mitigate pathogen transmission, decision-makers may be loath to implement effective biosecurity measures if they are concerned about public opposition to these measures. We found strong support across members of the public for biosecurity measures to mitigate pathogen transmission through the herpetological trade, namely increased quarantine and veterinary observation of herpetofauna imports, mandatory tests for diseases of concern for imported herpetofauna, and best practices to reduce stress and improve the care of live herpetofauna during transport. Respondents’ values and their perceived susceptibility and sensitivity to different hazards associated with pathogen transmission by captive herpetofauna were key determinants of their support for biosecurity. Different messages should be tailored to members of the public with different values to elicit their support for biosecurity. Our results suggest that individuals with strong biospheric or altruistic values are likely to respond to messaging about the transmission of pathogens from captive herpetofauna to native animals, domestic animals, and humans as well as the ecological impacts associated with pathogen transmission (such as loss of biodiversity). Individuals with strong egoistic values are likely to respond to messaging about the economic and public health risks associated with pathogen transmission. When possible, communication about pathogen transmission should also provide suggested actions that individuals can take to enhance the effectiveness of government-implemented biosecurity.

Supporting information

Acknowledgments

We thank C. M. Romagosa and T. B. Waltzek for their valuable comments during the design of the survey. We thank M. J. Yabsley for his valuable comments during revision of this manuscript.