Date of Award

5-2018

Degree Type

Dissertation

Degree Name

Doctor of Philosophy (PhD)

Department

Forestry and Natural Resources

Committee Chair

Rod Williams

Committee Member 1

Elizabeth Flaherty

Committee Member 2

William Hopkins III

Committee Member 3

Jason Hoverman

Abstract

Translocations often use captive-reared animals to help bolster or re-establish wild populations. Captive-rearing provides safety and ample amounts of food so animals can be released as larger, older individuals. However, captive environments are highly dissimilar from wild conditions and may deprive animals of experiences that promote normal development. Naïveté to natural stimuli can result in inappropriate or dangerous behaviors following release, elevated predation in the wild, increased disease susceptibility, and ultimately, failed translocation efforts. Eastern hellbenders (Cryptobranchus alleganiensis alleganiensis) have experienced precipitous declines over the past few decades in Indiana and have been reduced to a single, low-density population in the Blue River. Captive-rearing and translocations are underway; however, previous efforts have had variable success, leaving this population extremely vulnerable to extirpation. I examined the efficacy of using semi-natural conditions in a captive setting to advance eastern hellbender head-starting techniques and improve standard rearing practices. I developed novel forms of environmental enrichment, predator conditioning, and bioaugmentation wherein I reared hellbenders with riverine-like water current (Chapter 1), predator kairomones (Chapter 2), and free-flowing river microbiota (Chapter 3). My goal was to combat captive-reared hellbenders naïveté to wild conditions and better prepare hellbenders to specific threats they will encounter in a natural river. Hellbenders are commonly reared in aquaria that lack environmental stimuli and because of their inexperience with moving water may be more susceptible to downstream movement following release. I investigated the effects of rearing hellbenders with and without moving water on their body morphology and swim performance (Chapter 1). After 18 months, I found hellbenders reared in moving water had more shallow tails and better swim performance during simulated flood events. My data suggest that the addition of water current to hellbender rearing

environments produces a streamlined tail form, acclimates hellbenders to moving water, and improves their ability to reach upstream refugia. Although some anti-predator behaviors are innate, many animals are brought into captivity at young ages before they have ever encountering a predator. Captive hellbenders identify predatory fish as threats, but may be more vulnerable to predation and stress without previous exposure to them. I investigated the use of predator conditioning to prepare hellbenders, behaviorally and physiologically, to the presence of a common riverine predator, largemouth bass (Micropterus salmoides, Chapter 2). I reared hellbenders for 30 days with and without continuous exposure to largemouth bass kairomones and heterospecific alarm cues. I found conditioned hellbenders became less active and had lower metabolic rates compared to unconditioned individuals. These data demonstrate that predator conditioning induces behavioral avoidance tactics that likely reduce predator detection and physiological changes that lower energetic demands. Captive environments often lack natural microbial reservoirs, have filtration systems that remove excess microbes, and are maintained in hygienic ways to prevent the spread of disease. Subsequently, captive hellbenders may have depauperate microbial populations, lack symbiotic bacterial species, and subsequently may have increased disease susceptibility and reduced immune potential compared to wild conspecifics. In order to prepare hellbenders for natural free-flowing bacteria found in wild environments, I devised a novel bioaugmentation method. I exposed three-year-old eastern hellbenders to river water in captivity, before releasing them into their natal river in Indiana (Chapter 3). I found treatment hellbenders increased alpha diversity and had distinct differentiation in the community composition on their skin after they were exposed to undiluted river water in captivity. My data showed strong evidence that hellbenders’ skin is being colonized by rare environmental OTUs and exposing hellbenders to river water is as an effective reservoir for bacterial colonization as release into the river. I also found suggestive evidence of an immune response among treatment hellbenders following river release, which may provide protection against the colonization of opportunistic species. If pre-exposed hellbenders have an advantage over control individuals because of microbial diversity and immune responses, then this novel technique could have beneficial effects on future translocation efforts. This dissertation provides critical information to advance head-starting techniques for hellbender captive-rearing programs. The presence of water velocities, predator kairomones, and free-floating river microbiota are all representative of natural conditions and effectively induced morphologic plasticity, altered behavior, and physiological changes that could positively influence hellbender survival upon release into the wild. Future work is needed to explore the effects of these novel methods, separately and in combination, on hellbender movement, habitat use, health, and survival following translocation into the wild. If rearing hellbenders with semi-natural conditions and environmental stimuli in captivity can improve the success of future translocations, incorporating these novel methods into head-start programs could have profoundly positive effects on hellbender conservation initiatives in Indiana and throughout the nation.

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