Abstract
Investigation into the causes underlying the rapid, global amphibian decline provides critical insight into the effects of changing ecosystems. Hypothesized and confirmed links between amphibian declines, disease, and environmental changes are increasingly represented in published literature. However, there are few long-term amphibian studies that include data on population size, abnormality/injury rates, disease, and habitat variables to adequately assess changes through time. We cultured and identified microorganisms isolated from abnormal/injured and repressed tissue regeneration sites of the endangered Ozark Hellbender, Cryptobranchus alleganiensis bishopi, to discover potential causative agents responsible for their significant decline in health and population. This organism and our study site were chosen because the population and habitat of C. a. bishopi have been intensively studied from 1969–2009, and the abnormality/injury rate and apparent lack of regeneration were established. Although many bacterial and fungal isolates recovered were common environmental organisms, several opportunistic pathogens were identified in association with only the injured tissues of C.a. bishopi. Bacterial isolates included Aeromonas hydrophila, a known amphibian pathogen, Granulicetella adiacens, Gordonai terrae, Stenotrophomonas maltophilia, Aerococcus viridans, Streptococcus pneumoniae and a variety of Pseudomonads, including Pseudomonas aeruginosa, P. stutzeri, and P. alcaligenes. Fungal isolates included species in the genera Penicillium, Acremonium, Cladosporium, Curvularia, Fusarium, Streptomycetes, and the Class Hyphomycetes. Many of the opportunistic pathogens identified are known to form biofilms. Lack of isolation of the same organism from all wounds suggests that the etiological agent responsible for the damage to C. a. bishopi may not be a single organism. To our knowledge, this is the first study to profile the external microbial consortia cultured from a Cryptobranchid salamander. The incidence of abnormalities/injury and retarded regeneration in C. a. bishopi may have many contributing factors including disease and habitat degradation. Results from this study may provide insight into other amphibian population declines.
Highlights
The amphibian decline controversy has focused on many factors that affect amphibian populations to varying degrees [1], including habitat loss and degradation, climate change, pollution, increased ultraviolet B (UV-B) radiation, direct exploitation, introduced species and disease, including infectious disease [2,3]
One bacterial species would represent the vast majority of the colonies from a given abnormal/ injured sample as exemplified by the known human pathogen Granulicatella adiacens, which represented 91% of the 163 bacterial isolates found on the blood agar plate associated with the North Fork of White River (NFWR) 139 lower lip sample
Many reasons for the decline in population and health of the Ozark Hellbender have been suggested, including flooding [39,49] amphibian harvesting [42], the use of the anesthetic MS-222 (Tricane) [50,51], the reintroduction and introduction of species including otters and trout [47,52], habitat alteration and degradation [53], disease including those having a genetic, chemical, or infectious etiology [36,41,48,50,51,53,54,55,56,57,58,59,60,61], and the interaction of these factors [47]. Many of these hypothesized causal agents of decline have been investigated to various degrees, yet disease research has largely been limited to B. dendrobatidis [59,60,61], and prior to our study, the microbial community associated with the abnormalities typifying the affected hellbenders had not been assessed
Summary
The amphibian decline controversy has focused on many factors that affect amphibian populations to varying degrees [1], including habitat loss and degradation, climate change, pollution, increased ultraviolet B (UV-B) radiation, direct exploitation, introduced species and disease, including infectious disease [2,3]. Evidence of disease in amphibian populations is not new, early literature on amphibian health in natural populations is quite scattered, deals primarily with anurans and/or local problems, or was initiated because of concerns related to supply and demand and decline of commercial harvest [4,5,6]. The review of mycoses of amphibians by Reichenback-Klinke and Elkan [8] primarily focuses on Basidiobolus ranarum and Saprolegnia parasitica and indicates the dearth of knowledge relating to the distribution and importance of microfungi associated with amphibians. With few exceptions, this void continued for the two decades [9,10,11,12]. The impetus for research on amphibian microbes became a major focal point of the 1st World Herpetology Congress in Canterbury, England in 1989, where herpetologists shared their observations on declining frog populations and developed initial strategies to investigate the potential problems
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