(The) Role of Physiological Ecology and Genomics in Amphibian Conservation

다국어 초록 (Multilingual Abstract)

The world's biodiversity is currently at a critical juncture, facing significant threats from climate change, habitat loss, and environmental pollution. Among the most affected are amphibians, key contributors to global biodiversity, now teetering on the brink of extinction. These creatures play a crucial role in wetland ecosystems, contributing to nutrient cycling and forming integral parts of food chains. The decline in amphibian populations highlights the severity of the biodiversity crisis and has garnered the attention of conservation biologists worldwide.
To effectively protect amphibians, a comprehensive understanding of their population sustainability is essential. This requires the development of management strategies based on ecological knowledge. A multidisciplinary approach, combining conservation physiology and genetics, is particularly valuable. Physiological studies, including nutrition, growth, metabolism, endocrinology, and disease research, provide insights into the challenges faced by amphibians and how they adapt to environmental changes. Genetic studies complement this by analyzing gene pools and gene flow, contributing to our understanding of population stability. Considering the unique life cycle of amphibians, particularly their distinct experience of metamorphosis among vertebrates, adds complexity to conservation efforts. Therefore, a thorough understanding of amphibians' diverse life stages is crucial for their conservation.
This study aims to integrate conservation physiology and genetics to establish a robust conservation framework for amphibians. It incorporates physiological tools such as host microbiology, endocrinology, and immunology, alongside veterinary examinations like blood biochemistry and radiology, areas not typically explored by amphibian specialists. Additionally, genetic analyses using microsatellite markers enhance our predictions of population viability. By intertwining these fields with behavioral ecology, developmental biology, wetland ecology, environmental engineering, and phenology, the study seeks to predict amphibian survival across various habitats and uncover their physiological adaptive mechanisms.
This thesis is structured into six chapters, with the first five chapters comprising fully published papers. Each chapter contributes to a comprehensive understanding of amphibian conservation, focusing on physiological, morphological, and genetic aspects.
Chapters 1 and 2 provide an extensive overview of physiological, morphological, and genetic benchmarks for field amphibians. Chapter 1 is dedicated to veterinary clinical examinations, which are crucial for accurately diagnosing conditions in amphibians. A key aspect of these examinations is the establishment of reference intervals (RIs) for precise interpretation and identification of abnormalities in individual animals. In this chapter, RIs for immunity, serum components, bone mineral density (BMD), and body composition were established for 151 male Pelophylax nigromaculatus. These analyses are not only replicable but also crucial for safely and accurately diagnosing the physiological condition of amphibians. The integration of these physiological analysis is instrumental in developing successful conservation strategies by identifying issues in various amphibian species.
Chapter 2 shifts the focus to the scope of frog populations, specifically analyzing the genetic and morphological structure and diversity of black-spotted pond frog populations within the Geum River watershed in South Korea. This study found no significant differences in the genetic structure of frog populations across 14 sub-watershed areas, indicating that these frogs represent a single genetic population. However, variations were observed in skull morphology between some sub-watershed areas. Interestingly, these morphological distance correlated with geographic distance rather than genetic distance. This finding is significant for habitat scoping and provides valuable insights for population management, conservation, and research.
Chapters 3 and 4 of the thesis focus on evaluating the sustainability of amphibian populations and exploring biological response to anthropogenic environmental factors. Especially, chapter three build upon the data and insights from Chapters 1 and 2, applying them to practical field scenarios.
Chapter 3 centers on the population management of anurans, assessing habitat suitability in relation to river structures and artificial levees. The chapter conducts genetic and physiological analyses of frog populations in riverine wetlands, comparing those in riverside areas between water channels and river levees with those in protected lowlands between river levees and human settlements. The findings suggest that enhancing habitat connectivity is crucial. Frogs in riverside areas may not be at a disadvantage in terms of population genetic diversity or physiological conditions, but they could be genetically isolated due to the presence of levees. This chapter underscores the importance of genetic and physiological data in understanding complex habitats and managing amphibian populations within ecosystems.
Chapter 4 aims to identify the physiological and behavioral impacts on anuran populations resulting from eco-friendly strategies for wind energy production. Specifically, it examines the interconnected behavioral, physiological, and immunological responses of Japanese tree frogs (Dryophytes japonicus) to wind turbine noise during their breeding season. The results indicate that turbine noise may lead to decreased immunity in these frogs as a result of an energy trade-off for increased calling rates, rather than acting solely as a physiological stressor causing a direct increase in corticosterone levels. This reduced immunity, stemming from the physiological response to noise, has the potential to alter the disease epidemiology within the population and foster new adaptive patterns in these habitats. These findings demonstrate that physiological analysis is effective in identifying various stressors affecting amphibians and can be instrumental in elucidating complex biological mechanisms.
Chapters 5 and 6 of the thesis delve into the physiological impacts associated with the complex life history of amphibians, focusing on their responses to both external and internal factors.
Chapter 5 aims to comprehensively investigate how variations in growth rate and gut bacterial communities in amphibians are influenced by temperature differences during the complex process of metamorphosis. The study examines the role of both exogenous and endogenous factors in altering the gut microbiota of tadpoles. The findings suggest that intrinsic biological systems often have some significant influence on organism homeostasis and variation than external environmental pressures. While the impact of environmental factors can vary in magnitude and type, the process of metamorphosis in tadpoles is shown to have a profound effect on their biology, particularly in terms of microbial interactions. This research advances our understanding of host-microbiome interactions and highlights the complexity of amphibians' life history.
Chapter 6 assesses the relationships among food resources, the gut bacterial community, and the host physiology of frogs, taking into account phenological variations and life histories. The results indicate that the gut microbiome may serve as a link between food source and the physiological status of frogs. Furthermore, phenology appears to strengthen the relationship between gut microbiota and physiological status in anurans. This study is significant as it contributes to our understanding of the interplay between the physiological state and gut microbiota in ectothermic animals. It also provides valuable insights for future research on microbial communities and their detailed response processes.

국문 초록 (Abstract)

기후변화와 서식지 파괴, 환경 오염과 같은 생태계의 위협 요소들이 서로 복잡하게 상호작용하면서 전 세계의 생물다양성이 전례 없는 위기에 직면하고 있다. 특히 양서류는 전 세계적으로 심각한 멸종 위기에 처해있는 지구 생물다양성의 중요한 부분이다. 양서류는 습지 생태계에서 영양 염류의 효율적인 순환과 먹이 사슬의 연결과 같은 중요한 역할을 수행하는데, 이들의 감소는 생물다양성 위기를 더욱 부각시킨다. 이를 고려하여 많은 보전생물학자들이 양서류의 감소에 주목하고 이를 효과적으로 보호하기 위한 방법을 연구하고 있다.
양서류의 효과적인 보전을 위해서는 개체군의 지속 가능성을 평가하고 생태학적 현상에 대한 이해를 기반으로 관리 전략을 수립하는 것이 필수적이다. 이를 위해 보전생리학과 보전유전학의 목표를 통합하는 다학제적 접근 방식이 활용될 수 있다. 영양, 신진대사, 성장, 내분비, 질병 상태 등을 포함한 생리 분석은 양서류 개체군이 경험하는 위협 요인을 추적하는 데 유용하다. 이러한 분석을 통해 양서류가 변화하는 환경에서 경험할 수 있는 반응과 적응 과정을 식별할 수 있다. 또한, 유전학적 접근 방식은 유전자 풀의 구성과 유전자 흐름을 기반으로 한 개체군의 안정성을 평가하는 데 도움이 된다. 종합적으로, 두 분야의 목표를 융합함으로써 개체군의 건강과 안정성을 파악하여 지속 가능성을 증진시킬 수 있다. 양서류의 생활사가 변태를 경험하는 유일한 척추동물 중 하나로, 이러한 복잡성은 보전 전략과 관리 방안 수립을 어렵게 만든다. 따라서 개체군 상태의 평가뿐만 아니라 양서류의 복잡한 생활사를 고려하여 생태학적 현상을 이해하는 것도 양서류 보전에 기여할 수 있다.
이 연구는 보전생리학과 보전유전학의 접근 방식을 통합하여 양서류의 효과적인 보전 방법을 제시하고 체계적인 보전 관리에 기여하는 것을 목표로 한다. 양서류학자들이 일반적으로 사용하지 않는 혈액 생화학 및 방사선학과 같은 수의 임상검사를 포함한 숙주의 미생물학, 내분비학, 면역학과 같은 생리학적 분석이 소개된다. 더불어 마이크로새틀라이트 마커를 사용한 유전학적 분석이 개체군의 지속 가능성 예측을 향상시키기 위해 결합된다. 결과적으로, 이러한 분야들은 행동학, 발생생물학, 습지 생태학, 환경공학, 현상학 등 여러 분야와 결합하여 다양한 환경에 놓인 양서류 개체군의 지속 다양성을 예측할 뿐만 아니라, 양서류가 경험할 수 있는 주요 생태학적 현상에 따른 생리학적 적응 메커니즘을 이해하는 데 사용된다.
논문은 총 여섯 개의 장으로 구성되어 있으며 이 중 다섯 개의 장은 출판이 완료된 논문으로 구성되어 있다. 각 장에서는 개체군의 생리 상태와 유전적 양상에 초점을 맞추어 양서류 개체군을 평가하고 체계적인 보전을 위한 이해 증진의 공통 목표를 가진다.
첫 번째 장과 두 번째 장에서는 현장의 양서류에 대한 생리·형태·유전학적 정보 구축에 대한 내용으로 구성된다. 첫 번째 장에서는 양서류의 상태를 정확하게 진단하기 위해 필수적인 수의 임상 검사 (veterinary clinical examination)에 대해 다룬다. 이러한 검사의 핵심적인 측면은 개체 단위의 특이 사항을 정확하게 진단하고 식별하기 위한 기준 범위 (reference interval)를 설정하는 것이다. 이 장에서는 151마리의 수컷 참개구리 (Phelophylax nigromaculatus)에 대한 선천 면역, 혈청 성분, 체성분 및 골밀도의 기준 범위를 설정하였다. 이러한 분석은 양서류의 생리 상태를 안전하고 정확하게 진단하기 위해서도 효과적으로 사용될 수 있다. 특히 여러 종류의 생리학적 분석을 통합하는 것은 다양한 양서류 종에서 나타날 수 있는 문제를 식별하게 도와주며, 이를 통한 효과적인 양서류 관리와 보전에 기여할 수 있다.
두 번째 장에서는 무미양서류 개체군의 범위에 초점을 맞추어 국내의 금강 유역 내 참개구리 개체군의 유전적·형태적 다양성과 구조의 차이를 분석하고자 하였다. 본 연구에서는 14개 유역에 따라 참개구리 개체군의 유전적 구조의 차이가 나타나지 않았으며, 이는 이 지리적 범위 안의 참개구리 개체군들이 단일 유전적 집단으로 구성된다는 것을 보여준다. 그러나 두개골의 형태는 일부 개체군 사이에서 나눠지는 것을 확인할 수 있었다. 이러한 형태학적 거리는 유전적 거리보다는 지리적 거리와 상관성이 있었다. 이 결과는 개체군의 서식지 범위 지정에 유용하게 사용될 수 있으며 개체군 관리와 보전 및 연구에 중요한 통찰력을 제공한다.
세 번째 장과 네 번째 장에서는 인위적인 환경 요인에 대한 양서류 개체군의 지속가능성을 평가하고 생물학적 반응 기작을 연구하는 데에 중점을 둔다. 특히 세 번째 장에서는 첫 번째 장과 두 번째 장에서 획득하였던 생리 및 유전 정보를 사용하여 현장 개체군의 상태 평가를 적용한다.
세 번째 장은 하천의 구조와 인공 제방과 관련된 서식지 적합성을 평가하여 무미양서류 개체군의 관리 방안을 수립하는 데에 중점을 둔다. 이 연구에서는 수로와 하천 제방 사이의 제외지 개체군과 제내지 개체군에 대한 유전 및 생리학적 상태 비교를 수행한다. 연구 결과는 서식지의 연결성을 강화하는 것이 제방에 영향을 받을 수 있는 참개구리 개체군의 관리에 효과적일 수 있다는 것을 시사한다. 제외지의 참개구리 개체군은 유전적 다양성이나 생리 상태가 저하된 상태로 나타나지는 않지만, 제방의 존재를 통해 이들 개체군은 일시적인 유전적 고립을 경험할 수 있다. 이 장에서는 복잡한 서식지를 이해하고 생태계 내의 양서류 개체군들을 관리하는데 있어 유전학적·생리학적 정보의 중요성을 강조한다.
네 번째 장은 풍력 에너지 생산을 위한 친환경 전략이 무미양서류 개체군에 미치는 생리적·행동적 영향을 확인하는 것을 목표로 한다. 구체적으로, 번식기 동안 풍력 터빈 소음에 영향을 받은 청개구리 (Dryophytes japonicus)의 행동, 생리, 면역학적인 연결 반응을 확인하고자 하였다. 연구 결과는 풍력 터빈 소음이 단일 생리학적 스트레스 요인으로 작용하기보다는 울음소리 속도 증가를 위한 에너지 교환의 결과로 청개구리의 면역 저하를 유발하는 것을 보여주었다. 소음에 대한 생리학적 반응으로 인해 감소된 면역력은 개체군의 질병 역학을 변화시키고 이러한 서식지에서 새로운 적응 양상을 조성할 가능성이 있다. 이러한 발견은 생리학적 분석이 양서류에 영향을 미치는 다양한 스트레스 요인을 식별하기 위해 효과적으로 사용될 수 있으며 복잡한 생물학적 기작을 밝히는 데에 도움이 될 수 있음을 보여준다.
다섯 번째 장과 여섯 번째 장은 외인성 및 내인성 요인에 대한 양서류의 반응에 초점을 맞추어, 양서류의 복잡한 생활사와 관련된 생리학적 영향을 파악한다.
다섯 번째 장은 양서류의 성장률과 장내 세균 군집의 변화가 복잡한 변태 과정에서 온도 차이에 의해 어떻게 영향을 받는지 포괄적으로 조사하는 것을 목표로 한다. 이 연구는 올챙이의 장내 미생물을 변화시키는 데 있어서 외인성 요인과 내인성 요인 모두의 역할을 조사한다. 연구 결과는 내재적 생물학적 시스템이 외부 환경 압력보다 종종 유기체의 항상성과 변이에 더 중요한 영향을 미치는 경우가 있다는 것을 보여준다. 환경 요인의 영향은 다양한 규모와 유형으로 변화될 수 있지만 올챙이의 변태 과정은 특히 미생물 상호 작용 측면에서 생물학적 시스템에 중대한 영향을 미치는 것으로 나타났다. 이 연구는 숙주와 미생물의 상호작용에 대한 이해를 증진시키고 양서류 생활사의 복잡성을 강조한다.
여섯 번째 장에서는 생리학적 변이와 생활사를 고려하여 참개구리에서 식량 자원과 장내 세균 군집, 숙주 생리 상태 사이의 관계를 평가한다. 연구 결과는 장내 미생물 군집이 먹이원과 개구리의 생리학적 상태 사이의 연결고리 역할을 할 수 있음을 나타낸다. 더욱이, 현상학은 장내 미생물군과 무미양서류의 생리학적 상태 사이의 관계를 강화시키는 것으로 보인다. 이 연구는 변온동물의 생리학적 상태와 장내 미생물군 사이의 상호작용을 이해를 증진시킬 수 있다는 점에서 중요하다. 또한 미생물 군집과 상세한 반응 과정에 대한 향후 연구를 위해 귀중한 통찰력을 제공한다.

목차 (Table of Contents)

• I. Chapter 1. Reference Intervals in Combined Veterinary Clinical Examinations of Male Black-Spotted Pond Frogs (Pelophylax nigromaculatus) 1
• 1.1. Introduction 1
• 1.2. Materials and Methods 4
• 1.3. Results 10
• 1.4. Discussion 16
• II. Chapter 2. Genetic and Morphological Pattern of the Black-Spotted Pond Frog (Pelophylax nigromaculatus) in Watershed Areas of the Geum River in South Korea 22
• 2.1. Introduction 22
• 2.2. Materials and Methods 25
• 2.3. Results 35
• 2.4. Discussion 46
• III. Chapter 3. Assessment of Habitat Suitability in Riverine Wetland Using Genetical and Physiological Analysis of Anurans (Pelophylax nigromaculatus) 49
• 3.1. Introduction 49
• 3.2. Materials and Methods 53
• 3.3. Results 66
• 3.4. Discussion 79
• IV. Chapter 4. Wind Turbine Noise Behaviorally and Physiologically Changes Male Frogs 86
• 4.1. Introduction 86
• 4.2. Materials and Methods 90
• 4.3. Results 104
• 4.4. Discussion 115
• V. Chapter 5. Tadpole Growth Rates and Gut Bacterial Community: Dominance of Developmental Stages Over Temperature Variations 121
• 5.1. Introduction 121
• 5.2. Materials and Methods 123
• 5.3. Results 129
• 5.4. Discussion 139
• VI. Chapter 6. Phenology of Anuran Strengthen the Response and Relationship Between Their Physiology and Gut Bacterial Community 144
• 6.1. Introduction 144
• 6.2. Materials and Methods 148
• 6.3. Results 155
• 6.4. Discussion 167
• VII. Overview conclusion 174
• VIII. References 178

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