Herps and plant health

Amphibians and reptiles contribute to overall plant health through seed dispersal and pollination and as predators of crop pests (Valencia-Aguilar et al., Reference Valencia-Aguilar, Cortés-Gómez and Ruiz-Agudelo2013; Hocking and Babbitt, Reference Hocking and Babbitt2014). Herps can serve as pollinators when they move from flower to flower, drinking nectar and inadvertently transporting pollen for example Xenohyla truncate (de-Oliveira-Nogueira et al., Reference de-Oliveira-Nogueira, Souza, Machado, Figueiredo-de-Andrade, Mônico, Sazima, Sazima and Toledo2023). In another example, the dusky lizard (Liolaemus belii) has been shown to be an important seed disperser of a barberry species native to Chile (Celedón-Neghme et al., Reference Celedón-Neghme, San Martin, Victoriano and Cavieres2008). This is significant because berberine, a popular dietary supplement with medicinal benefits, comes from barberry plant species. As predators, 78% of the South American toad’s (Rhinella arenarum) diet includes arthropods that damage crops, and it is reported that the loss of R. arenarum and other amphibians will decrease this biological pest control for soybean crops (Attademo et al., Reference Attademo, Peltzer and Lajmanovich2005).

Herps and animal health

An interdependency exists between herpetofauna and other wildlife in their ecosystems. Larval amphibians can occur in incredibly high densities in some ecosystems and are likely to have significant effects on ecosystem functions, including primary productivity, through changes in the food web (Seale, Reference Seale1980). They can act as primary consumers, detritivores, predators and even cannibals, improving water quality of both wild and farm ponds and in turn affecting domestic and farm animal health (Gibbons et al., Reference Gibbons, Winne, Scott, Willson, Glaudas, Andrews, Todd, Fedewa, Wilkinson, Tsaliagos, Harper, Greene, Tuberville, Metts, Dorcas, Nestor, Young, Akre, Reed, Buhlmann, Norman, Croshaw, Hagen and Rothermel2006). Reptiles can also impact farm animal health. For example, Caiman species can control aquatic snails that serve as intermediate hosts for the trematode Fasciola hepatica, which damages the liver of infected cattle and sheep (Valencia-Aguilar et al., Reference Valencia-Aguilar, Cortés-Gómez and Ruiz-Agudelo2013). Herps can also be impacted as a cascade effect; for example, declines in neotropical frogs and tadpoles can result in significant declines of frog-eating snake populations (Zipkin et al., Reference Zipkin, DiRenzo, Ray, Rossman and Lips2020).

Herps and human health

One of the most common notions connecting herptile species and human health is the detrimental presence of poison in amphibians and reptiles. Venomous species inject toxin by bite (e.g., cobra) or sting, while humans handling poisonous species may ingest, inhale or absorb toxins (e.g., poison dart frog). Injection or ingestion of toxins may result in illness or death. Furthermore, while herptile species can be a food source for humans (e.g., frog legs), there is concern over their potential to carry multidrug-resistant strains of important human pathogens like E. coli and Acinetobacter spp. similar to other meats (Morrison and Rubin, Reference Morrison and Rubin2020). The mechanisms of such antimicrobial resistance in wildlife species remain unclear but may be tied to persistence of antimicrobial residues in domestic animals and the environment (Vittecoq et al., Reference Vittecoq, Godreuil, Prugnolle, Durand, Brazier, Renaud, Arnal, Aberkane, Jean-Pierre, Gauthier-Clerc, Thomas and Renaud2016). Given the gravity of emerging antimicrobial resistance, further investigation into drug-resistant microbes and wild herpetofauna is warranted. Human health and well-being benefit from herptile species, including the development of cancer therapies, cardiovascular therapies and other treatments (Table 1; Bordon et al., Reference Bordon, Cologna, Fornari-Baldo, Pinheiro-Júnior, Cerni, Amorim, Anjolette, Cordeiro, Wiezel, Cardoso, Ferreira, Oliveira, Boldrini-França, Pucca, Baldo and Arantes2020).

Table 1. Examples of connections between herptile species and human health

Turtles

Turtles play a prominent role in the creation story of several indigenous peoples and tribes across the Americas. The Iroquoi, Ojibwe, Algonquin, Cree and others believe that North and Central America were formed on the back of a large turtle that Great Mother Aataentsic landed on after falling through a hole in the sky (Pearce, Reference Pearce2005). Contemporarily, turtles are also responsible for ecotourism booms to watch and participate in the conservation of sea turtle species during nesting on beaches (Jacobson and Lopez, Reference Jacobson and Lopez1994).

Snakes

Many traits that are associated with snakes have been likened to human traits - for example the sinuous coils of a snake’s body are often related to human hair, becoming a symbol of richness, wealth and prosperity in 4th century Roman culture (Lazarou, Reference Lazarou2018). In one Aboriginal dreaming story, the rainbow serpent is referred to as a creator and, like the rainbow, frequently associated with water and rainfall. The rainbow serpent is a widespread tradition in pre-colonial Australian societies, depicted in the rock art of the Waayni people from Northwestern Queensland (Taçon, Reference Taçon2008).

Even to this day, the rod or staff of the Greco-Roman god of healing and medicine, Asclepius, is used as a symbol of health care. Evidence suggests that the non-venomous European Aesculapian snake (Zamenis longissimus), which derives its name from this god, was allowed to roam freely in “healing temples” in ancient Greece and was even used for healing superficial skin lesions (Demetrioff, Reference Demetrioff2020). The association of snakes with wisdom is also propounded through many early cultures, including Hinduism, where the god Shiva, who typically wears a snake around his neck, represents wisdom (Stanley, Reference Stanley2008).

Frogs, toads and salamanders

Many neotropical societies view frogs as good-luck charms or signs of fertility, dating back thousands of years (Valencia-Aguilar et al., Reference Valencia-Aguilar, Cortés-Gómez and Ruiz-Agudelo2013). Amazonian indigenous tribes have used skin secretions of several Dendrobatid frogs to rub on their bodies to gain power or to experience pain and euphoria (Valencia-Aguilar et al., Reference Valencia-Aguilar, Cortés-Gómez and Ruiz-Agudelo2013). In addition, secretions can be used in making “curare,” a poison used in hunting and medicine (Valencia-Aguilar et al., Reference Valencia-Aguilar, Cortés-Gómez and Ruiz-Agudelo2013). In Asia, frogs and toads are associated with wisdom and magic in Chinese and Japanese cultures (DeGraaff, Reference DeGraaff1991).

Impacts of anthropogenic environmental degradation and contamination on herps

Global ecosystem changes of the Anthropocene have impacted herptiles more profoundly than any other vertebrate taxa (Barnosky et al., Reference Barnosky, Matzke, Tomiya, Wogan, Swartz, Quental, Marshall, McGuire, Lindsey, Maguire, Mersey and Ferrer2011). For amphibians, especially, their shared terrestrial and aquatic life histories, permeable skin and adaptation to species-optimal thermal, precipitation and UV radiation conditions make them a good sentinel species for environmental health and “canaries in the coalmine” for environmental degradation (Hopkins, Reference Hopkins2007). In many areas of the globe, amphibians have been among the first taxa to show population-wide responses to genotoxic and teratogenic environmental contaminants like pesticides, herbicides, agricultural runoff, sewage, and pharmaceutical and industrial effluent (Egea-Serrano et al., Reference Egea-Serrano, Relyea, Tejedo and Torralva2012). Population-wide health impacts of environmental contaminants in amphibians, like atrazine, have triggered re-evaluation of legally allowed levels of chemicals in wastewater and environmental effluent to protect environmental health as well as public health (Roy, Reference Roy2002). These chemicals have the potential to induce genotoxic and teratogenic changes in exposed humans as well.

Land-use change driven by human influence on the environment is a major driver of global biodiversity loss (Isbell et al., Reference Isbell, Gonzalez, Loreau, Cowles, Díaz, Hector, Mace, Wardle, O’Connor, Duffy, Turnbull, Thompson and Larigauderie2017). For herpetofauna specifically, habitat loss and degradation are considered crucial drivers of species declines (Ford et al., Reference Ford, Hunt, Haines, Lewis, Lewis and Green2020). These declines will have profound implications for other organisms and ecosystems.

Impacts of climate change on herp health

Climate change is associated with warming global temperatures, changing precipitation patterns, sea level rise and increased extreme weather events. These shifts in climate are altering the habitats that amphibians and reptiles reside in, and, as such, suitable environments for their survival may be shrinking (McMenamin et al., Reference McMenamin, Hadly and Wright2008; Luetdke et al., Reference Luedtke, Chanson, Neam, Hobin and Maciel2023). Climatic events have been linked to local population extinctions, the predicted dispersal of herpetofauna to areas outside of their normal ranges, and projections that more herptile species will be listed as endangered, threatened or vulnerable (Olson and Saenz, Reference Olson and Saenz2013; Luetdke et al., Reference Luedtke, Chanson, Neam, Hobin and Maciel2023). In Table 2, we review the potential impacts of climate change on herptile species.

Table 2. Summary of potential and demonstrated impacts of climate change on Herptile Health

Rises in ambient temperatures may influence reptile biodiversity, especially in species with temperature-dependent sex determination because rises in temperature may skew sex ratios to levels that cannot sustain populations (Valenzuela et al., Reference Valenzuela, Literman, Neuwald, Mizoguchi, Iverson, Riley and Litzgus2019); this is especially the case for chelonian diversity (Ihlow et al., Reference Ihlow, Dambach, Engler, Flecks, Hartmann, Nekum, Rajaei and Rödder2012). It has been suggested that larval development may be the most vulnerable amphibian life stage affected by climate shifts due to more regular droughts and the general rise in water temperature in amphibian breeding habitats (Sinai et al., Reference Sinai, Glos, Mohan, Lyra, Riepe, Thöle, Zummach and Ruthsatz2022). Climate change (i.e., high temperatures and increased drought in some regions) may be beneficial or harmful to herptile species in terms of changing pathogen dynamics, pathogen pollution by invasive species, water stress and trophic mismatch.

Pathogen dynamics

The herptile host–pathogen relationship is highly temperature-dependent and likely one of the most significant drivers determining infectious disease outcomes (Rohr et al., Reference Rohr, Raffel, Romansic, McCallum and Hudson2008). Higher temperatures, in both live animal exposure experiments and wild populations, are associated with increased disease occurrence and severity (Price et al., Reference Price, Leung, Owen, Puschendorf, Sergeant, Cunningham, Balloux, Garner and Nichols2019). It has been hypothesized that increased drought will reduce the prevalence of the amphibian skin-eating fungus, Batrachochytrium dendrobatidis (Bd), because the pathogen is dependent on freshwater for reproduction and survival (Fisher et al., Reference Fisher, Garner and Walker2009). Others argue that Bd is amplified by drought conditions (Pounds et al., Reference Pounds, Fogden and Campbell1999) because infection of the pelvic patch, important for rehydration, would make frogs more vulnerable during dry periods. For reptiles, seasonal climate variations that alter overwintering conditions and ambient air temperatures, likely play a crucial role in pathogen transmission and disease culmination, which has been suggested for snake fungal disease (Albecker and McCoy, Reference Albecker and McCoy2017). In another reptile study, warmer temperatures resulted in overall higher ectoparasite infections in wild common lizard (Zootoca vivipara) females, though the lizard’s color variety/morphotype varied the rate of infection (Wu et al., Reference Wu, Miles, Richard, Rutschmann and Clobert2022). The degree to which climate alterations affect disease outcomes of individual pathogen-exposed amphibians and reptiles and how this translates to a landscape scale and/or population level, still needs to be further elucidated.

Hydric stress

While many reptiles are adapted to arid and mesic environments with limited water availability, hydric stress can influence thermoregulatory behavior (Ladyman and Bradshaw, Reference Ladyman and Bradshaw2003), influence sex ratios in offspring (Dupoué et al., Reference Dupoué, Lourdais, Meylan, Brischoux, Angelier, Rozen-Rechels, Marcangeli, Decencière, Agostini and Le Galliard2019) and stagnate reproduction (Dezetter et al., Reference Dezetter, Le Galliard, Guiller, Guillon, Leroux-Coyau, Meylan, Brischoux, Angelier and Lourdais2021). These scenarios can often lead to reproductive failure and decreases in recruitment (Chandler et al., Reference Chandler, McLaughlin, Gorman, McGuire, Feaga and Haas2017). All amphibians rely on availability of freshwater or moisture for reproduction regardless of life history. Because most amphibians display a biphasic life history, eggs, tadpoles and metamorphs are particularly vulnerable to the direct effects of drought such as mortality from desiccation or dehydration (Li et al., Reference Li, Cohen and Rohr2013). Somewhat counterintuitively, reptiles under hydric stress show enhanced components of immune function (Brusch et al., Reference Brusch, Mills, Walman, Masuda, Byeon, DeNardo and Stahlschmidt2020), which may be a result of adaptation to arid environments, or to counteract the reduced immune capacity of reptiles maintaining lower body temperatures when under hydric stress (Ladyman and Bradshaw, Reference Ladyman and Bradshaw2003). This phenomenon deserves further study to investigate how it may influence host–pathogen dynamics.

Trophic mismatches

Changes in phenology of herpetofauna food sources could result in trophic mismatches upon spring emergence (Kharouba et al., Reference Kharouba, Ehrlén, Gelman, Bolmgren, Allen, Travers and Wolkovich2018), unless phenology shifts in herpetofauna are synchronous with shifts in their food sources. Conversely, winters are predicted to be shorter in some parts of the globe (Räisänen et al., Reference Räisänen, Hansson, Ullerstig, Döscher, Graham, Jones, Meier, Samuelsson and Willén2004), which could be beneficial for reptiles and amphibians that hibernate, as long as food sources are available. Experimental work suggested that a shorter, warmer winter was beneficial for survival and body mass changes during hibernation for common toads (Bufo bufo) (Üveges et al., Reference Üveges, Mahr, Szederkényi, Bókony, Hoi and Hettyey2016). Alternatively, climate change may result in prolonged estivation or behavioral refugia time which could lead to reduced foraging or breeding windows and ultimately population declines (Sinervo et al., Reference Sinervo, Méndez-de-la-Cruz, Miles, Heulin, Bastiaans, Villagrán-Santa Cruz, Lara-Resendiz, Martínez-Méndez, Calderón-Espinosa, Meza-Lázaro, Gadsden, Avila, Morando, De La Riva, Sepulveda, Rocha, Ibargüengoytía, Puntriano, Massot, Lepetz, Oksanen, Chapple, Bauer, Branch, Clobert and Sites2010).

Developing a holistic approach to manage emerging herp threats

To apply a true “One Health” approach, we must expand our thinking beyond pathogens/diseases of concern and include overall health and determinants of health for monitoring and conservation actions. For example, the approach taken by Wittrock et al. (Reference Wittrock, Duncan and Craig2019) that considers a “Determinants of Health” model for caribou and sockeye salmon. This model, which has roots in public health, considers biotic, abiotic and social contributions that factor into health outcomes (Wittrock et al., Reference Wittrock, Duncan and Craig2019). Can we foresee something similar for amphibians and reptiles, to broaden our approach to managing health with a holistic, systems-based approach? How do we accomplish this with limited resources dedicated to herpetofauna? Are there existing systems already in place that can be utilized? The following are a few selected examples that might be included in One Health approaches.

Engaging participatory science into herp monitoring programs

OH JPA Activity 6.3.8 - Engage with citizen science on data collection for monitoring the health of the environment to inform action.

It is widely accepted that in an environment where professional resources for species monitoring are increasingly scarce, community scientists are of greater importance. Despite concerns about the robustness of data collected in this way and the biosecurity practices employed, participatory science is making a significant contribution in many regions (Schmeller et al., Reference Schmeller, Henry, Julliard, Gruber, Clobert, Dziock, Lengyel, Nowicki, Déri, Budrys, Kull, Tali, Bauch, Settele, Van Swaay, Kobler, Babij, Papastergiadou and Henle2009). Perhaps, increasing the engagement of the public may prove useful, raising awareness of the plight of herpetofauna and giving the public a role in herpetofauna health and conservation, ultimately elevating the popularity status of herpetofauna despite their cryptic nature (e.g., see Figure 1).

Figure 1. Examples of how Citizen Science can be incorporated into herptile One Health approaches. Adapted from https://www.usgs.gov/media/images/illustration-participatory-science-usgs-ecosystems-mission-area.