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Will Cognitively Challenging Headstarted Amphibians with Ecologically Appropriate Stimuli Lead to Greater Repatriation Success?

Ecology and Diversity
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Will Cognitively Challenging Headstarted Amphibians with Ecologically Appropriate Stimuli Lead to Greater Repatriation Success?

Michael J. Lannoo 1 Vicky Poole 2 Tim Herman 3 Robert Hill 4 Allan P. Pessier 5 Ruth Marcec-Greaves 6 Mark Vassallo 7 David Vardukyan 7 Michael Andrus 7 Wynona Shellabarger 7 Brad Barr 7 Claire Lannoye-Hall 7 Nathan J. Engbrecht 8 Rochelle M. Stiles 9,*

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1
Indiana University School of Medicine—ISU, Terre Haute, IN 47809, USA
2
Fort Worth Zoo, Fort Worth, TX 76110, USA
3
Indoor Ecosystems, Whitehouse, OH 43571, USA
4
Zoo Atlanta, Atlanta, GA 30315, USA
5
College of Veterinary Medicine, Washington State University, Pullman, WA 99164, USA
6
Lincoln Children’s Zoo, Lincoln, NE 68502, USA
7
Detroit Zoological Society, Royal Oak, MI 48067, USA
8
Indiana Department of Natural Resources, Bloomington, IN 47401, USA
9
San Francisco Zoological Society, San Francisco, CA 94132, USA
*
Authors to whom correspondence should be addressed.

Received: 14 May 2026 Revised: 12 June 2026 Accepted: 18 June 2026 Published: 26 June 2026

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© 2026 The authors. This is an open access article under the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/).

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Ecol. Divers. 2026, 3(2), 10008; DOI: 10.70322/ecoldivers.2026.10008
ABSTRACT: The frequent failure of headstarting programs suggests we are overlooking important factors in amphibian reintroduction science. Since many repatriation efforts are in vain, such programs can become difficult to justify from a cost-benefit perspective (chronic failure also takes its toll on staff morale), ultimately working against the goals of conservation programs. The question of how to properly prepare amphibian larvae or juveniles for reintroduction and persistence in the landscape is of utmost importance. Here, we offer a previously unconsidered perspective that is predicated on the idea that amphibians, being vertebrates, have forebrain-based cognitive capabilities aligned along the nucleus accumbens-based reward system and the amygdaloid nuclei-based fear system. Experiences uploaded by the ventromedial pallium as memories are thought to be tagged as accumbens-based ‘good’ or amygdala-based ‘bad’, and stored as (relatively) long-term memories; as such, amphibians are said to be salient creatures. The necessarily nurturing nature of zoo husbandry protocols naturally works against young amphibians acquiring ecologically realistic life lessons, especially when these forebrain reward and fear circuits are developing. For example, in zoos, food provisioning eliminates the reward associated with searching for and then finding food, and the emphasis on survival in captivity means headstarted animals released into the wild have no opportunity to experience fear. Such under-stimulated reward/fear circuits poorly prepare headstarted animals for life in the wild. It follows that kindling this circuitry as it develops with ecologically relevant stimuli will better prepare animals for life following release into the wild. To the extent that realistic headstarting protocols call for sacrificing a few animals to enhance the experiences of the remaining many, they will no doubt be resisted by institutions. But we have two choices here: keep doing things the way we have been doing and expect different outcomes, or experiment with new ideas based on a broader understanding of these animals—ideas such as these we are now proposing—to improve the success of repatriation efforts.
Keywords: Reintroduction; Captive-rearing; Conservation; Release; Predator training; Survival; Zoo; Aquarium

1. Introduction

Members of the vertebrate class Amphibia appear especially vulnerable to environmental challenges posed by the Anthropocene, in large part because they can neither flee far nor fast from the many forms of environmental degradation currently affecting Earth’s tropical, temperate, and subpolar ecosystems [1,2,3,4]. Further, most amphibians have complex life histories and therefore must rely on both high-quality aquatic and terrestrial ecosystems to complete their life cycles, which, using Boolean logic [5], has an innately higher probability of failure than when survival is dependent on the quality of a single habitat type (but see [6]). For these reasons, and because amphibians form critical links in the trophic structure affecting reptiles, birds, and mammals, amphibian conservation has become a global priority.

One goal of modern amphibian conservation efforts has been to reverse declines by re-establishing extirpated populations after ecosystems have been restored or recovered [7,8,9,10]. However, the survival of animals following release into the wild has been generally poor, and in too many cases, these efforts have failed to meet their goal of re-establishing populations [8,11,12,13]. There have been many proposed causes for these failures, which include unsuitable habitat at the release site causing death or dispersal, animals being preyed upon immediately, genetic issues ranging from drift to bottlenecks, translocation shock, and disease [7,8,9,11,12,14,15,16,17]. Our purpose here is not to revisit these causes but rather to introduce an additional factor that, similar to genetic issues, is externally unobservable but may explain the failure of repatriation efforts when such failures cannot be attributed to other causes. Our idea comes from the fact that amphibians are vertebrates and therefore have cognitive functions that develop during certain critical periods when neuronal circuits form. We propose that, in the absence of appropriate ecological stimulation during these critical periods, animals may not develop the necessary cognitive tools needed to successfully meet the post-release demands of a novel and threatening environment. In essence, we challenge the assumption that healthy captive headstarted animals will always innately adjust and thrive after release. To address this issue, we propose re-imagining how we raise headstarted animals. In short, we suggest that providing them with ecologically realistic and challenging situations as their forebrains develop fear and reward circuits should better prepare them for life in the wild and increase post-release survivorship.

2. The Role of Zoos in Headstarting Programs

The animals seeding repatriation (definition following [9]) efforts often come from captive-rearing and release (i.e., headstarting) programs, which are typically centered in zoos and aquariums [11,18]; but see [19]. For the purposes of the present discussion, amphibian headstarting involves collecting eggs from clutches laid in the wild, transporting them to a rearing facility, hatching them, and raising the larvae under controlled conditions with the goal of increasing survivorship during early, vulnerable life-history stages [20]. While there has been considerable success in raising healthy headstarted animals for reintroduction programs (i.e., if these animals remained in captivity, they would live for years, possibly a decade or more), as mentioned above, the survival of animals once released into the wild has been generally poor and/or underreported, and may be further obscured by publication bias that overrepresents successful outcomes [20,21].

3. Identifying Reasons for Headstarting Failures

Because repatriated amphibians can be difficult to monitor, it is rare that the reasons for their failure to establish are known. When causes are known, they tend to be based on ecological or genetic factors. A few examples illustrate this point. Predation can rapidly eliminate released cohorts, such as Cane Toads (Rhinella marina) consuming newly metamorphosed Peltophryne juveniles or gartersnakes preying on juvenile Yosemite Toads (Anaxyrus canorus; pers. comm. T. May). Habitat degradation may also drive failure; for instance, stream siltation can destroy the rock crevices that Eastern Hellbenders (Cryptobranchus alleganiensis) require for cover and nesting sites, while the introduction of predaceous fish can also wipe out Hellbender cohorts [22]. Large-scale disturbances, such as wildfire (reviewed by [23]), and genetic limitations may further constrain population recovery. Other factors include low survival of developmentally malformed tadpoles [24] or newly metamorphosed frogs. Disease represents another well-documented driver of repatriation failures: in Sierra Nevada and Mountain Yellow-legged Frogs (Rana sierrae, Rana muscosa), individuals sourced from Batrachochytrium dendrobatidis-naïve populations can succumb to chytridiomycosis following release (unpubl. data, L. Jacobs; unpubl. data, San Francisco Zoo and partners). Again, these are not the situations we will be considering here. Instead, we focus on instances where headstarted animals are released into habitats without obvious dangers or deficits yet are not successful, or where headstarted animals are introduced into a depleted population yet do not successfully supplement that population.

What can we do to increase the survivorship of headstarted amphibians released into the wild? As we emphasize to caretakers participating in the long-running Amphibian Taxon Advisory Group Amphibian Management School, the survivorship and wellbeing of individuals in captivity are tied to recreating critical elements of a species’ natural history (see also [8,11,25,26]). This is especially true of headstarted animals destined for release into the wild. For example, compared with diurnal releases (convenient for humans), nocturnal releases (more aligned with natural amphibian activity patterns and misaligned with common amphibian predators) often increase survivorship [8,27]. Similarly, placement of individuals into predator-avoidant microhabitats (i.e., soft releases) buys time for newly released animals to acclimate and become oriented to their surroundings [13,15,20,28,29,30].

The problem with raising headstarted animals in captivity is that modern zoo husbandry techniques typically emphasize raising healthy, stress-free animals by meeting an animal’s every need, including offering an adequate and balanced diet, ensuring optimum ranges of temperature and ideal water composition, reducing exposure to harmful chemicals such as chlorine and phosphorus, isolating animals from pathogens, minimizing intraspecific aggression, and excluding predators [18,26].

This approach works well when raising animals for display or education. But when headstarting animals for release in nature, providing for every need without requiring animals to work towards meeting these needs, for example, by searching for high-quality food, discovering optimal physical and chemical conditions, interacting with aggressive conspecifics, and learning to avoid predators, likely has consequences for animals destined to be released into the wild and asked to fend for themselves. Further, even when calls to provide an enriched environment are heeded, such efforts are rarely tied to any real-world situations [11,12]. Here we suggest that offering ecologically realistic challenges and choices to headstarted larvae should better prepare them for release into nature. Unlike other workers who have offered a similar suggestion [8,11,12,31], we base our assertion on the idea that headstarted animals must be appropriately stimulated when developing the nervous system circuitry that will underlie all their future behavior (see also [32,33]).

4. Amphibian Cognition and Its Development

Amphibian survival following stress-free headstarting would approximate wild survival if Tinbergen and Ewert’s views of amphibians as anoetic (non-thinking) animals were true [34,35,36]. Tinbergen [34] believed amphibians were “simple reflex machines” (see also [37]). Similarly, Ewert [35,36] felt that in amphibians, key stimuli (innate releasing mechanisms) activated fixed patterns of behavioral responses (i.e., reflexes), much like a key fitting a lock [38,39,40]. That is, once sensory receptors have identified an object and a location, a pre-programmed circuit in the midbrain tectum is “dialed up” (the metaphor here is a rotary telephone, reflecting the technology of the day). Further, Ewert [35,36] felt individual tectal locations existed for all possible stimulations and positions, meaning an amphibian’s response to any situation is genetically, reflexively programmed into their nervous system circuitry.

If Tinbergen [34] and Ewert’s [36] perspective is correct, amphibians are unable to learn, and they could be raised as if they were plants. But we now know amphibians have cognitive abilities [41]. They form associations and memories, the basis of learning. For example: (a) European Spadefoot (Pelobates cultripes) tadpoles learn to associate non-threatening stimuli with conspecific alarm cues and subsequently consider these benign stimuli threatening [42]; (b) experiences change the temperament of Rana arvalis tadpoles [43]; (c) repetition of a stimulus results in Wood Frog (Rana sylvatica) tadpoles remembering it longer [44]; (d) calling American Bullfrog (Rana catesbeiana) males learn to recognize (i.e., remember) and ignore the calls of adjacent males [45]; and (e) as Red-backed Salamanders (Plethodon cinereus) become more familiar with a novel prey species they become more efficient foragers on that species [46].

Amphibians are also masters at remembering and navigating landscapes, and will use different senses and strategies to locate sites important to them [47,48,49,50]. For example, during navigation: (a) adult Marsh Frogs (Pelophylax ridibundus) use magnetic fields [51]; (b) adult Terrestrial Toads (Rhinella arenarum) use geometric and feature cues [52,53,54]; and (c) adult Green and Black Poison Dart Frogs (Dendrobates auratus) use a cognitive map [55].

Further, amphibians are aware of their environment. For example, after prescribed burns eliminate their vegetative cover, adult Crawfish Frogs (Rana areolata) spend more time in their burrows compared to frogs in intact ecosystems, a behavior Engbrecht and Lannoo [56] interpret as minimizing exposure to potential predators (if true, such anticipation is a cognitive ability Tinbergen [34] and Ewert [36] would dismiss as an amphibian impossibility).

Amphibians are also socially aware. For example, Wood Frog (Rana sylvatica) tadpoles learn to avoid predators by watching the reactions of other Wood Frog tadpoles [57]. And, consistent with the observations of Bee et al. [45], mentioned above, breeding American Bullfrogs are highly attuned to social situations. Young (small) males must decide whether to (a) join a breeding chorus (lek), where they have a higher probability of mating but face competition and perhaps injury from larger males (high risk/high reward), or (b) become a satellite male, remaining on the periphery where they might ambush and mate with a female moving towards the lek (low risk/low reward). Further, when females are ready to breed, they locate the lek of large males and assess the number and location of peripheral satellite males. If there are few satellite males, females approach the lek on the water surface. If there are numerous satellite males, females dive underwater and surface in or near the lek to avoid being amplexed by smaller, perhaps less fit, males, which could mean wasting an entire year’s reproductive effort (pers. comm. R. Howard) [41,58].

Amphibians are likewise self-aware. In their encounters with Eastern Gartersnakes (Thamnophis sirtalis), Crawfish Frog adults must assess their body size relative to the snake’s size to determine whether the snake is a potential predator (gartersnakes will prey on young Crawfish Frogs), a potential prey (Crawfish Frog adults are big enough to ingest a young gartersnake), or presents no danger or opportunity (these two species occasionally share burrows; [41]).

Finally, amphibian cognitive skills vary across species. Burmeister [59] compared Green and Black Poison Dart Frogs (Dendrobates auratus) with Túngara Frogs (Engystomops pustulosus) and found the more complex ecological and social environments of Poison Dart Frogs correlated with higher levels of gene expression tied to neurogenesis, synaptic plasticity, and cellular activity. This is an important concept not only when headstarting animals but also when considering the timing of their release (see below).

As with all cognitive abilities there are age-specific times—termed critical periods, sensitive periods, or developmental windows—in young vertebrates when the brain is particularly receptive to ecological and social stimuli [60,61,62,63,64,65,66,67]. Critical periods arise during the development of sensory, associative, and motor circuits responsible for detecting and responding to particular stimuli. Exposure to appropriate stimuli during these developmental windows influences the number and strength of maturing synaptic connections in central nervous system circuits (e.g., [68]). If these synapses fail to form, axons retract, and the parent neurons, having no function and being energetically expensive, undergo programmed death, a process called apoptosis (e.g., [69]). A non-stimulated circuit that loses a high number of neurons to apoptotic death will not function normally. As Ohmer et al. [70] note, a tadpole’s environment has lasting effects on its juvenile and adult behavior.

5. The Senses Driving Critical Periods

Tadpoles in the wild are naturally exposed to relevant stimuli during these critical periods and therefore typically form an appropriate number of functional synapses (if they didn’t, they would behave abnormally and be rapidly selected against). Examples of relevant stimuli include light, detected by photoreceptors in the eyes, the pineal gland, and by melanophores in the tail; sound, detected by hair cells in the inner ear; water displacements, detected by hair cells arranged in epidermal lateral line organs; and ambient temperature, assessed by receptors and free nerve endings in the epidermis [71]. Tadpoles also sense a variety of organic and inorganic molecules using an array of four chemosensory systems: the principal and accessory olfactory systems, taste, and specialized epidermal chemosensory cells called stiftchenzellen (‘spike cells’) [72]. Olfaction is generally regarded as distant smell, taste is oral smell (produced most robustly by macerated food), and chemosensation, as assessed by stiftchenzellen is thought to encompass ‘vague’ smell [71,72].

With the exception of olfaction, information from each of these senses courses through the brainstem and is filtered and tuned before reaching the forebrain telencephalon; olfactory cues project directly into the telencephalon. Based on neuroanatomy, Striedter and Northcutt [73] suggest anurans have an olfactory dominated telencephalon. Ethologists and physiologists agree [74,75,76]. Petranka [76] found Bufo americanus tadpoles are attracted to ‘rich’ food patches and avoid areas containing alarm substances (schreckstoff). When tested on whether attractive food or schreckstoff was the stronger stimulus, bufonid tadpoles did not choose between them but rather exhibited an intermediate response [76]. Other examples of tadpoles relying on olfactory cues include the observation that bufonid tadpoles learn the odor of their invertebrate prey [77], and while hylid tadpoles use kairomones to detect the presence of a predator [78], ranid and bufonid tadpoles use schreckstoff to detect the act of predation [79,80,81,82,83]. Ranid tadpoles exposed to schreckstoff increase their corticosterone production within the neuroendocrine stress axis, overseen by the hypothalamus [84].

Olfaction is also important in other situations. Bufonid tadpoles use chemical cues to recognize kin [85], rhacophorid tadpoles are attracted to chemical cues associated with females depositing trophic eggs (unfertilized eggs laid to provide nutrition for tadpoles in impoverished environments such as epiphytic bromeliad tanks) [47,86,87], and older Cane Toad tadpoles chemically suppress viability in younger conspecific tadpoles [88].

Vision is also an important sense in tadpoles, especially for detecting overhead predators ([36]; see also [89]). Herons and egrets hunt along wetland shorelines searching for tadpoles in shallow water. Tadpoles use visual cues, especially motion, to escape this form of predation. Further, recent experimental work demonstrates the importance of integrating multiple sensory modalities in shaping antipredator responses. Hammond et al. [90] combined visual and olfactory cues to expose headstarted Mountain Yellow-legged Frog (Rana muscosa) tadpoles and metamorphosed frogs to a gartersnake (physically separated but both visible and chemically detectable). Predator-exposed tadpoles exhibited altered morphology, slower development (an approximately 14 d delay), reduced movement, and weighed less than controls. Predator training also improved post-release survival, although this training did not carry over across metamorphosis and had to be reinforced in later life history stages.

Every tadpole sensory system except lateral line mechanoreception persists (with modifications) through metamorphosis and carries over into adulthood [71]. Memories acquired from stimulating these sensory systems during the tadpole stage are likely uploaded by the telencephalic ventromedial pallium and remembered as positive (reward) or negative (threat) experiences mediated by the nucleus accumbens or amygdala, respectively [41,58,59,65,73,91,92]. This circuitry is as far as we will go in ascribing higher-order cognitive processes to amphibians. For example, we are uncomfortable with the idea that amphibians have emotions [93], although, when assigning ‘good’ or ‘bad’ tags to memories, we agree that amphibians have salience. We are now also uncomfortable with using the term ‘personality’ to identify an amphibian’s position on the Shy-Bold Continuum and prefer to use ‘temperament’ instead [29]. Such human-based vocabulary implies shared neurological causes between human and amphibian behavior when we know human neocortex, especially the prefrontal cortex, is a cognitive gamechanger.

Tadpole brain anatomy remains understudied. There is, for example, no ‘go to’ atlas of the tadpole brain that one can refer to as a baseline neuroanatomical reference. Further, when early neuroembryologists studied tadpole brains, it was with the assumption that the anuran central nervous system formed linearly from embryo through larval stage to adulthood [94,95]. That is, early workers treated frog neuroembryology as if an amphibian were just another terrestrial vertebrate, with brains growing along a single developmental vector towards adulthood. A more modern and realistic perspective incorporates the fact that amphibians have a biphasic life history and that both tadpole and adult life history stages, while constrained by being phases of the same organism, can to a great degree develop and evolve separately in response to functional/ecological demands [96,97,98,99,100,101]. This is the basis of ‘Starrett’s Rule’, which states that the plainest of adult frogs often have the most bizarre tadpoles, while the strangest adults typically have the most mundane tadpoles [97,102]. The few studies on tadpole brain growth show that most of the development of the hindbrain medulla occurs prior to metamorphosis [103] and that at metamorphosis, the forebrain diencephalon widens and the telencephalon elongates as new neurons are added [104]. Absent high-resolution information on tadpole brains and their development, the best proof for the presence of critical periods during amphibian development remains behavioral evidence.

Given the presence of critical periods and the fact that most anuran tadpoles and adults are very different animals, the retention of tadpole memories per se may be less important to a post-metamorphic frog than the role experiences play in developing the forebrain reward and threat circuits. A headstarted tadpole that has never searched for food has never been rewarded for seeking and finding food. If circuits mediated by the nucleus accumbens require rewards following effort to properly develop, such headstarted tadpoles may not create the circuitry necessary to motivate feeding in post-metamorphic juveniles or adults. Similarly, a headstarted tadpole that never knows fear may miss the developmental window for the establishment of robust fear circuits mediated by the nucleus accumbens. Absent such circuitry, post-metamorphic frogs may not be able to elicit a fear response adequate to the reality of living in an environment that is, as Tennyson noted, “red in tooth and claw” [105].

In addition to the possibility of neural risk/reward circuits failing to develop properly, headstarting situations can reverse an animal’s reaction to natural risk/reward stimuli (see also [11]. Ewert [36] summarized European Toad responses to other animals as:

 

small and moving = prey: approach;

  

large and looming = predator: flee.

  

In a reversal of “Ewert’s Rule”, headstarted animals can quickly learn to associate food (reward) with large, looming objects (i.e., people). In this scenario, rather than stimulating amygdaloid fear circuits, large, looming objects stimulate nucleus accumbens reward circuits. In the wild, a headstarted amphibian that approaches a predator, thinking it will be fed, is rarely given the opportunity to make this mistake twice.

6. The Failure of Vertebrate Headstarting Programs Is Not Restricted to Amphibians

The reduced fitness of headstarted vertebrates released into the wild is not limited to amphibians; this problem occurs in all vertebrate classes. For example, it has been observed in captive-raised salmon from wild stocks [106,107,108], gamebirds [109], and to a lesser extent, mammals [110], including European Otters (Lutra lutra) [111], Scandinavian Roe Deer (Capreolus capreolus) [112], and Black-footed Ferrets (Mustella nigripes) [113]. This suggests a common cause or set of causes related to the lack or exposure to or experience with situations encountered once captive-reared animals are released into nature.

7. Providing Appropriate Scenarios Simulating Natural Conditions to Headstarted Amphibians

We are not the first to recognize that environmental enrichment can stimulate cognition in amphibians. Burghardt [93] chastised zookeepers for not enriching the lives of their captive amphibians and reptiles. His solution centered on the concept of “controlled deprivation,” meaning he understood that even the best captive environments do not completely reflect natural ecosystems; therefore, it becomes important to provide a subset of the natural world that offers the most enriching experiences. In emphasizing such enrichment, however, Burghardt [93] did not distinguish between artificial and natural enhancement. We believe this difference is important.

With the concept of developing the neural circuitry during critical periods in mind, we propose offering headstarted tadpoles a range of ecologically realistic situations, as follows:

(1)

Periodically expose tadpoles to wetland water from the landscape where they will be released. This not only introduces them to natural food and predator odors, but swimming in such water may help build natural microbiotic gut flora, which in turn influences neurodevelopment and behavioral responses through the microbiota-gut-brain (MGB) axis [114]. (Note: wetland water can serve as a vector for pathogens, including ranaviruses and Batrachochytrium dendrobatidis [Bd]; programs should mitigate this risk and consult with veterinary and regulatory partners.)

(2)

Offer different quality food options and allow tadpoles to choose. This should stimulate the nucleus accumbens reward circuits as they develop. Because tadpoles naturally graze throughout the water column, they distribute food across benthic, midwater, and surface zones. Further, offer these food items at different times of the day and night; in nature, prey rarely present themselves on a regular schedule.

(3)

Periodically introduce natural aquatic predators (invertebrates such as giant water bugs, predaceous diving beetles, and dragonfly naiads [115,116]; vertebrates such as salamander larvae) and allow them to prey on a few tadpoles [117,118,119,120]. This will introduce kairomones and schreckstoff into the tadpoles’ environment and should stimulate telencephalic amygdaloid fear circuits as they are developing. Indeed, predator-induced phenotypes, likely mediated by hormonal and autonomic cues originating from the forebrain hypothalamus, are commonly observed in hylid tadpoles [121,122,123].

If the introduction of live predators is not feasible, exposure to predator-associated sensory cues may still promote learning, as demonstrated using combined visual and olfactory cues in headstarted Mountain Yellow-legged Frogs [90]. Indeed, the Indiana Hellbender Recovery Team, based at Purdue, is exposing a subset of their headstarted larvae to schreckstoff and will be monitoring post-release survivorship in exposed and unexposed animals (Unpublished Final Report for Grant T7R27 submitted to the Indiana Department of Natural Resources in 2023; see also [30]).

An early idea among zookeepers was that briefly introducing predators to captive animals decreased lethargy, which they felt somehow decreased stress [11,124,125]. While we question this positive relationship between lethargy and stress, we know predator-induced stress (i.e., fear) increases corticosterone production within the neuroendocrine stress axis, which involves the amygdaloid nuclei [84].

(4)

Randomly fly large objects [119] over rearing tanks as recommended by Hayes et al. [11], and while doing so, introduce schreckstoff. This pairing of visual and chemical cues will condition tadpoles to avoid large, moving objects overhead.

(5)

In temperate species, vary water temperatures across the range of tadpole tolerances [126]. In nature, when cold fronts roll through, tadpoles of spring breeding guild species can temporarily find their wetlands iced over [127]. In addition to reflecting natural environmental variability, temperature fluctuations can confer physiological benefits and, in some species, may be necessary for normal development (e.g., Foothill Yellow-legged Frog [Rana boylii], pers. comm. S. Kupferberg and D. Minier). Beyond physiology, temperature variability may also influence behavior and cognition; Oborová et al. [66] found that temperature extremes heightened exploratory behavior in Alpine Newts (Ichthyosaura alpestris), and exploration is a cognitive function.

(6)

Vary dissolved oxygen (DO) levels for tadpoles that possess developed lungs. Shallow wetlands containing macrophytes exhibit a daily cycle of DO variation, as these submerged plants photosynthesize in daylight and respire at night [127]. In these wetlands, DO levels are highest in late afternoon/early evening, often reaching supersaturated levels, and lowest at sunrise, when a combination of both plant and animal respiration creates hypoxic, and sometimes anoxic, conditions. Tadpoles with lungs and access to the water surface have little difficulty with low DO levels; they will gulp air and fill their lungs with atmospheric oxygen. In addition to reflecting natural environmental variability, an animal’s response to DO fluctuations might confer physiological benefits necessary for normal development. Even if this cannot be proven at this time, what is inarguable is amphibians raised under natural conditions exhibit levels of survivorship and recruitment sufficient to maintain populations or establish new populations, while animals raised artificially, in captivity, rarely manage this [8]. Given this reality, our contention is the nearer captive-rearing programs come to mimicking the physical, chemical, and biological challenges animals find in nature, including DO extremes, the more likely they will be successful in the wild.

(7)

Vary water levels to mimic evaporative losses and rainfall gains. Seasonal and semi-permanent wetlands are dynamic, variable systems that present challenges to developing amphibian brains that in turn influence the development of forebrain risk/reward circuits. In many temperate systems, single-season tadpoles experience progressive drying during mid- to late summer, often accompanied by increasing temperatures. In some species, these drought conditions can serve as a developmental cue; experimentally simulating these conditions—by reducing water levels while increasing temperature—can accelerate or trigger metamorphosis. For example, in Sierra Nevada Yellow-legged Frogs (Rana sierrae), drought simulation can successfully encourage metamorphosis in tadpoles that may otherwise require multiple years to complete larval development (unpubl. data, San Francisco Zoo and partners). More broadly, variation in temperature and hydrology influences growth and development in ranids.

(8)

The best solution to successfully headstarting may be to release tadpoles into their target wetlands as soon as possible [9]. Gosner Stage 25 tadpoles should be large enough to escape most vertebrate gape-limited predators, and swim fast enough to outpace most invertebrate predators. This suggestion is especially relevant for species like Túngara Frogs that appear to truncate forebrain neurogenesis [59]. In contrast, species that exhibit an extended period of neurogenesis, such as Poison Dart Frogs [59], might have the neuronal plasticity to adapt more quickly once released into the wild. Such an extended period of neurogenesis might also be found in juveniles of species that naturally never have the opportunity to react to an environment before finding themselves in one, such as direct developing species in the genera Plethodon and Eleutherodactylus [128] and live bearers in the genus Nectophrynoides [129].

(9)

Finally, what works for one species may fail in another, even when these species are closely related [130]. For example, Midland Chorus Frog (Pseudacris triseriata) tadpoles focus on feeding, while closely related and often syntopic Spring Peeper (P. crucifer) tadpoles focus on avoiding predators [117]. Relyea [131] exposed tadpoles of six anuran species to five different predator species and found that each tadpole species exhibited different responses to the same predator species. The morphological, behavioral, and ecological diversity encompassed by amphibians is staggering. Anuran amphibians alone comprise 57 families encompassing ~7843 species [4]. Each frog species must have some feature—molecular, morphological, physiological, or behavioral—that makes it unique. Anuran novelty includes aquatic, terrestrial, arboreal, or subterranean lifestyles; locomotory capabilities that include swimming, walking, jumping, and gliding; internal or external fertilization; egg masses that are laid aquatically, terrestrially, or arboreally; parental care that consists of maternal provisioning, egg carrying, tadpole transport, and egg incubation; generalist or specialist approaches to feeding; pigmentation patterns that emphasize camouflage, are aposematic, or vary to match the background; calling synchronously or asynchronously; philopatry; toxicity; cocoon building; and water conservation measures that use behavior (microsite selection) or behavioral physiology (e.g., waxy lipid secretions the frog spreads over its body) [132,133,134].

This adult variation is compounded by differences in tadpole morphology, behavior, and ecology, which also varies widely. For example, Orton [96] describes four basic types of tadpoles (see also [100]) while Amin and colleagues [135] have proposed an additional Type V based on the tadpoles of Lepidobatrachus laevis.

Given this variation in anuran morphology, ecology, and behavior, anuran brains must be considerably more variable than neuroanatomists working under a ‘scala natura’ approach were willing to acknowledge, although thankfully (we are reminded of the quote: “Funeral by funeral, theory advances”, attributed to Max Planck) this perspective is changing [58,136,137,138,139]. Brain variation in the telencephalon suggests cognitive variation (see [33,59]. As Bräuer et al. [140] emphasize, there is not ‘one cognition’.

Many of these recommended actions might be accomplished at most institutions, though they may require some updating of existing protocols, securing additional funding, and collaborating with ethologists and field biologists. In some cases, facilities may be resistant to adopting these changes unless they are requested or required by governing bodies (e.g., USFWS, state agencies). Most actions require approval by Institutional Animal Care and Use Committees (IACUCs) and permitting divisions of state and federal agencies.

While varying environmental parameters and diet should not seriously challenge husbandry protocols, introducing predators and allowing limited mortality may encounter serious resistance. This will vary by institution, as AZA-accredited facilities are not monolithic. Proposals that include sacrificing animals for the greater good will require strong justification and supporting evidence, including potentially a directive from the managing body of the program. Another option would be to “farm out” headstarted animals to conservation or university partners, following proper IACUC protocols or research committee reviews, thereby allowing flexibility to try “novel” concepts, such as challenging tadpoles to survive in a more natural setting to better prepare them for life in the wild.

8. Standard Framework

Rather than have the above recommendations come across as hardline prescriptions, we suggest considering each one of them as hypotheses to be tested as part of a larger repatriation research program coordinated across zoos. The goal is not to replace existing protocols. Rather, it is to evaluate the efficacy of different enrichment protocols in improving post-release survival and to allow institutions to develop best practices for captive populations marked for headstart. To aid this evaluation, we suggest standardizing a simple experimental structure that applies across scenarios both before and after release, which is categorized as follows:

Treatment vs. Control Groups: Divide animals into at least two groups: one experiencing the proposed ecological stimulus (treatment), and one reared under standard husbandry conditions (control).

Standardized Pre-release Assessments: Where feasible, evaluate behavioral or physiological responses prior to release. These may include foraging latency or efficiency, response to predator-associated cues (e.g., reduced activity or refuge use), exploratory behavior, growth, development, or body condition. These measures serve as indicators of whether the treatments are influencing behavior in the theorized direction.

Post-release Monitoring: Mark and identify individuals by treatment group and track short-term survival, site retention, dispersal patterns, and habitat use. This data will reflect whether pre-release differences translate into improved survival in the wild.

Comparative Evaluation: Evaluate effectiveness by comparing treatment and control groups across both pre- and post-release metrics.

9. Applying This Framework to Specific Testable Scenarios

To test scenario 1, institutions could expose one group of animals to wetland water, another to filtered water. Before releasing these animals into the wild, analyze gut microbial communities and compare between the two groups (and perhaps with wild counterparts from the wetland water source). Mark animals according to treatment and record survivorship during follow-up surveys.

To test scenario 2, feed one set of larvae different food items on variable feeding schedules with a non-uniform food presentation, feed another group with the standard practice of ubiquitous food inundation on a repeating schedule, and monitor growth while animals are in captivity. Prior to release, mark animals according to treatment and record survivorship during follow-up surveys.

If studies like this are done for each of the above scenarios, and post-release survivorship is enhanced, it would be wise to develop a set of husbandry guidelines (with variations and caveats) for headstarted animals that are distinct from the currently established husbandry guidelines for animals that will remain in captivity (e.g., [141]). Individually, these experiments may yield modest or contextually dependent results. However, if multiple institutions adopt similar frameworks and track a shared set of outcome metrics, collective data could clarify which interventions are most effective. In this way, the scenarios proposed here are not intended as fixed protocols, but as a foundation for a coordinated research effort to refine amphibian headstarting practices.

10. Conclusions

Zoos and aquariums play a critical role in headstarting amphibians for release into the wild with the goal of either re-establishing extirpated populations or augmenting depleted populations. While a few successes have been realized, and are rightfully celebrated, most of these efforts have been disappointing. There are many reasons for these failures, but in most cases the cause(s) remain unknown. This can be particularly frustrating when outwardly healthy amphibians are released into apparently intact landscapes containing critical ecosystems (e.g., wetlands for breeding, uplands for feeding, and overwintering sites). To address this problem, we propose incorporating our knowledge of vertebrate brain development into amphibian headstarting protocols. That is, we suggest that while current headstarting protocols designed to provide for every animal need and comfort succeed in raising healthy animals for exhibit or education, they fail to stimulate forebrain fear and reward circuits as they develop, and therefore fail to provide post-release animals with neuronal circuits ready to meet the challenges and uncertainties faced by living life in the wild. To facilitate these modifications, we propose exposing headstarted animals to: variations in food availability and quantity; predators or their chemical cues; and variations in water quality and quantity. Further, we recognize the stunning amount of variation that exists among the more than 8000 species of amphibians, and understand this means that protocols demonstrated to work in one species may fail in others, even among closely related species.

Acknowledgments

The authors constitute the current faculty and adjuncts of the Association of Zoos and Aquariums’ (AZA’s) Amphibian Management School (https://www.aza.org/calendar/event/5595301), which meets biennially at the Detroit Zoological Society’s National Amphibian Conservation Center (https://detroitzooblog.org/tag/national-amphibian-conservation-center/). Over the past decade, instructors informally discussed how to enhance the survivorship of captive-reared animals released into the wild. During the 2026 course these discussions intensified and became focused, resulting in the creation of this manuscript. Our perspectives towards amphibian headstarting and the framework we suggest for implementing them are our professional opinions and do not represent any policies or standards established by the AZA. If we have seen farther, it is because we are standing on the shoulders of giants. Bob Johnson, Joe Mendelson, Jenny Pramuk, Ron Gagliardo, Andy Odum, Diane Barber, and Shelly Grow are either former AZA Amphibian School instructors or colleagues who have contributed to the amphibian conservation mission of North American zoos and aquariums. We thank them for their decades-long inspiration, dedication, and friendship.

Author Contributions

Conceptualization, M.J.L., V.P., T.H., R.H., M.V., D.V., N.J.E., R.M.S.; Methodology, M.J.L., V.P., T.H., R.H., A.P.P., R.M.-G., M.V., D.V., M.A., W.S., B.B., C.L.-H., R.M.S.; Writing—Original Draft Preparation, M.J.L., V.P., T.H., R.H., M.V., D.V., N.J.E., R.M.S.; Writing—Review & Editing, V.P., T.H., R.H., M.V., D.V., N.J.E., R.M.S.

Ethics Statement

This article does not present research with ethical considerations and permits.

Informed Consent Statement

Not applicable.

Data Availability Statement

All other data produced in this study are provided in this manuscript.

Funding

This research received no external funding.

Declaration of Competing Interest

The authors declare they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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