Taiwanese pangolin (Manis pentadactyla pentadactyla) knowledge of reproductive physiology is imperative to maintaining a healthy ex-situ and in-situ population. Pangolins have been exhibited in zoos since the mid-1800s, but these prolonged years of captivity are facing a dilemma to propagate successful breeding in captivity. According to International Studbook and Formosan pangolin PHVA final report, this species' gestation length is confined in skepticism as well as has a low reproductive rate. Moreover, loss of neonates to stillbirths and incorrect maternal care during the critical period of pregnancies in captivity. As females do not exhibit clear signs of estrus or any specific sexual behavior and sometimes the signs of pregnancy have not been recognized to facilitate association between males and females to generate good breeding conditions. Pangolins have captivated the attention to unravel ecological and behavioral parameters, but reports on reproductive endocrinology are sketchy. I studied various reproductive physiology parameters (mating, pregnancy, gestation, and parturition) using serum and fecal samples procured from longitudinal sampling.
Fecal samples obtained enabled me to devise various metabolic forms of adrenal and gonadal steroids with the establishment of a pivotal study using the technique of Electrospray Mass Spectrometry (ESI-MS) existing in these endangered species of pangolins. The study also helped me unveil that Taiwanese pangolin does not show any significant differences among the functional categories of sub-adult (SA) and adult (A) in both males and females. However, the males showed significantly high differences in the level of fecal glucocorticoids compared with females.
The long-term hormonal examination of serum samples of pangolins from captivity illustrated significant differences in serum estradiol concentration between non-pregnant and pregnant females. However, both groups showed that estradiol's peak is synonymous with the annual mating season tied during the end of the year (November to January). The rising levels of progesterone in non-pregnant individuals during January suggest that estradiol and progesterone help in ovulation and estrus behavior in females. In pregnant females, the progesterone concentration sustained from January to September and drastically declined to mark the phase of parturition (October-December) in this species. In contrast, the non-pregnant females illustrated baseline concentration of serological progesterone apart from the estrus phase as marked in other closely related carnivores. This long gestation period of ~275 days (January-September) witnessed in pregnant females that it is highly probable that pangolins exhibit delayed implantation phenomena. The prolactin studies explained that pangolins exhibit a brief period of diapause because of the nursing behavior, which lasts from December to May.
Interestingly, males showed a seasonal pattern of testosterone levels. The endocrinological results suggest that the males engage in the mating behavior when the testosterone levels are the highest (October) in synchrony with females' parturition behavior. In summary, the hormonal evidence found both in male and female Taiwanese pangolin suggests that pangolins are seasonal breeders. This study also provided needed information on endocrinology and reproductive physiology for a hitherto unstudied species and provided a basis for a crucial contribution to future reproductive measures in conserving this enigmatic mammal.

Acknowledgment ........................................................................................................................ i
Abstract ..................................................................................................................................... iv
List of tables ...............................................................................................................................v
List of figures ............................................................................................................................ vi
Chapter 1: General Introduction ..............................................................................................1
1. Mammalian reproductive strategies ...................................................................................2
1.1.Ovulation ............................................................................................................................3
1.1.1. Spontaneous Ovulation .............................................................................................3
1.1.2. Induced Ovulation ...................................................................................................3
1.1.3. Polyovulation ...........................................................................................................4
1.2.Copulation ..........................................................................................................................5
1.3.Pregnancy ...........................................................................................................................6
1.4.Gestation .............................................................................................................................7
1.4.1. Delayed Implantation ...............................................................................................8
1.4.2. Delayed fertilization ...............................................................................................10
1.5.Parturition .........................................................................................................................11
1.5.1. Postpartum Estrus ...................................................................................................11
1.6.Breeding system ...............................................................................................................12
1.7.Pheromone system ............................................................................................................14
2. Functional association between gamete production, mating behavior and sex hormone secretion........................................................................................................15
3. Why is it essential to study the sex life of the world’s only scaly mammal?.......................17
4. Captive records on pangolin reproductive parameter …………………………………….21
5. Conservation breeding: A hope for dwindling pangolin population ……………………...24
6. Research aims and structure of this dissertation ………………………………………….27
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Chapter 2: The game-changer: A review on how the measurement of fecal steroid analysis changed the fate of hormone detection in wildlife……………………..31
Abstract…………………………………………………………………………………..32
1. Introduction ............................................................................................................................33
2. Revolution of fecal steroid studies and challenges ................................................................36
3. Collection, storage, and extraction of fecal samples for endocrine studies ...........................64
4. Fecal steroid metabolism ........................................................................................................66
5. Gonadal and adrenal fecal steroid metabolites to study wildlife biology ..............................70
6. Sampling methods ……………………………………………………………………….....73
6.1.Chemical identification of metabolites …………………………………………………73
6.1.1. Gas chromatography-mass spectrometry (GCMS) ...................................................73
6.1.2. Liquid Chromatography-mass spectrometry (LCMS) ..............................................74
6.1.3. High-pressure liquid chromatography (HPLC) ........................................................76
6.2.Immunogenic assays .........................................................................................................77
6.2.1. Enzyme-linked immunoassay (EIA) …………………………………………….77
6.2.2. Radioimmunoassay (RIA) ……………………………………………………….79
6.2.3. Chemiluminescence immunoassay (CLIA) ……………………………………...80
6.2.4. Radiometabolism…………………………………………………………………81
7. Other non-invasive sampling methods…………………………………………………….84
7.1.Urine…………………………………………………………………………………….84
7.2.Hair……………………………………………………………………………………...85
7.3.Saliva……………………………………………………………………………………87
8. Conclusion ………………………………………………………………………………...88
Chapter 3: Material and Methods ..............................................................................................90
1. Study Area ............................................................................................................................91
1.1 Taitung Coastal Mountain Range………...………………….…………………………..91
1.2 Taipei Zoological Park.………………….……………………..……………….………..85
1.3 Pingtung center for endangered wildlife..……………………………………………….86
viii
2. Study population ...................................................................................................................88
2.1. Study population A (Taitung Coastal Mountain Range) .......................................95
2.2. Study Population B (Taipei Zoological Park) …………………………………...92
2.3. Study Population C (Pingtung Rescue Center) ………………………….………93
3. Field Method ...................................................................................................................105
4. Fecal extraction method ………………………………………………………………..107
5. Extraction of blood serum………………………………………………………………108
6. Chemical sampling methodology ……………………………………………………...110
6.1. Steroidal standards and chemical reagents ……………………………………….110
6.2. Electron Spray Tandem Mass Spectrometry (ESI-MS/MS) Measurements……....111
6.2.1. Background……………………………………………………………………..111
6.2.2. Protocol…………………………………………………………………………114
6.2.3. Method evaluation……………………………………………………………..116
6.2.4. Physiological validation……………………………………………………….116
7.Immunogenic sampling methodology……………………………………………………..112
7.1. Chemiluminescence immunoassay (CLIA)……………………………………117
7.1.1. Background…………………………………………………………………….117
7.1.2. Protocol…………………………………………………………………………119
7.2. Estradiol (E2), progesterone (P4), and Testosterone (T) radioimmunoassay….121
7.2.1. Background…………………………………………………………………….121
7.2.2. Protocol…………………………………………………………………………122
8.Summary……………………………………………………………………………………127
Chapter 4: Electrospray Mass Spectrometry A Non-invasive method for endangered species: Identification endogenous steroids metabolite in feces of Taiwanese pangolin, (Order Pholidota, Family Manidae, Genus: Manis)………………………………………. 129
Abstract……………………………………………………………………………………130
1. Introduction……………………………………………………………………………….131
2. Materials and methods…………………………………………………………………….135
2.1 Study population……………………………………………………………………135
ix
2.2 Laboratory methods………………………………………………………………...136
3. Statistical data analysis………………………………………………………………...136
4. Results and discussion…………………………………………………………………137
4.1 Mass spectrometry…………………………………………………………………137
4.2 Analytical validation- precision in the extraction of extraction and purification of methanol extracts…………………………………………………...………………138
4.3 Selection of target analytes…………………………………………...…………….140
4.4 Physiological validation………………………………………………...…………..147
Chapter 5: Gonadal hormonal profile in Taiwanese pangolin (Manis pentadactyla pentadactyla) using serum: Evidence for delayed implantation …………………………152
Abstract………………………………………………………………………………...153
1. Introduction……………………………………………………………………………153
2. Materials and methods…………………………………………………………………158
2.1 Study population……………………………………………………………….158
2.2 Laboratory methods……………………………………………………………158
3. Data analysis…………………………………………………………………………...159
4. Results…………………………………………………………………………………159
4.1 Annual hormonal profile of pregnant and non-pregnant females……………..159
4.2 Annual hormonal profile of males……………………………………………...161
5. Discussion……………………………………………………………………………..162
5.1 E2 levels, seasonality in non-pregnant females………………………..……….162
5.2 Progesterone (P4) levels, corpus luteum, pregnancy, and parturition …………165
5.3 Evidence for delayed implantation during gestation…………………………...167
5.4 Reproductive behavior in males………………………………………………..172
5.5 Management implications………………………………………………………173
Chapter 6: Changes in serum prolactin concentrations during the annual cycle in female Taiwanese pangolin (Manis pentadactyla pentadactyla)……………………………………176
Abstract…………………………………………………………………………………….177
1. Introduction…………………………………………………………………………….177
x
2. Materials and methods………………………………………………………………….180
2.1 Study population…………………………………………………………………..180
2.2 Laboratory method………………………………………………………………...180
3. Results………………………………………………………………………………….181
4. Discussion……………………………………………………………………………....182
Chapter 7: General discussion and conclusion……………………………………………..188
1. Reproductive physiology of Taiwanese pangolin………………………………………189
2. Consideration of fecal samples to predict gonadal and adrenal steroid metabolic forms………………………………………………………………………..190
3. Non-invasive technique of electrospray ionization mass spectrometry for predicting metabolic forms in the fecal samples…………………………………..191
4. Estradiol and progesterone in female Taiwanese pangolin…………………………….194
5. Testosterone in male Taiwanese pangolin……………………………………………...196
6. Prolactin in female Taiwanese pangolin………………………………………………...197
7. Prolactin and ovarian steroids-Hormones of diapause………………………………….198
8. Reproductive physiology and conservation of Taiwanese pangolin……………………199
References…………………………………………………………………………….. 204

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