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«By NILMINI JAYASENA A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE ...»

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EFFECTS OF CHRONIC METHYLMERCURY EXPOSURE ON REPRODUCTIVE

SUCCESS, BEHAVIOR, AND STEROID HORMONES OF THE WHITE IBIS

(Eudocimus albus)

By

NILMINI JAYASENA

A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL

OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT

OF THE REQUIREMENTS FOR THE DEGREE OF

DOCTOR OF PHILOSOPHY

UNIVERSITY OF FLORIDA

2010 1 © 2010 Nilmini Jayasena 2 To my parents 3

ACKNOWLEDGMENTS

First and foremost, I wish to extend my sincere gratitude to my major adviser, Dr.

Peter Frederick for his support and guidance throughout this project. In addition to writing the initial proposal and getting funding, he was always there for advice, encouragement and help in herding ibises. He was truly a mentor in every sense of the word. I would also like to acknowledge the guidance and input of my supervisory committee, Drs. Iske Larkin, Madan Oli, Katie Sieving and Mel Sunquist. I received tremendous support from Dr. Michael Avery, Kandy Keacher and other personnel at the USDA Wildlife Research Center, Gainesville where the aviary was located. Dr. Marilyn Spalding gave valuable advice and training in various aspects of ibis health care. I wish to thank Dr. Lou Guillette and his lab for graciously allowing me use of his lab for radioimmunoassays. I would like to thank Dr. Ben Bolker and James Colee for statistical consultations. Many volunteers and assistants helped in collecting the data, I am grateful for all their help. I extend my special thanks to Nancy Montes, Teresa Bryan and Pilar Jaramillo for being friends as well as enthusiastic assistants. Leslie Straub and Bobbi Jo Sampson helped in general upkeep of the aviary and in keeping the birds happy. I would like to thank all the staff in the department, Caprice McRae, Monica Lindberg, Jennifer Vann, Claire Williams, Delores Tillman, Laura Hayes, Elaine Culpepper and Sam Jones for patiently and cheerfully helping me in numerous ways and clearing up many logistical problems.

A large number of friends helped me in numerous ways – a big thank goes out to all of them, especially to John Simon, Evan Adams, Kate Williams, Louise Venne, Ross Tsai, Fangyuan Hua, and Advait Edgaonkar. Many other friends helped me with words of encouragement, I would like to acknowledge Gamika Prathapasinghe, Gehan 4 Jayasuriya, Rasika Jinadasa, Harsha Ariyarathna, Naveen Wijesena, Bhagya Janananda and Uttara Munasinghe for their friendship and support throughout. I would be remiss if I did not mention all my teachers, especially my science teachers in primary and secondary school, as well as my lecturers at the University of Peradeniya, Sri Lanka, who kept me interested in science. Most of all, I wish to acknowledge my parents and sister for all their love, encouragement, guidance and support given throughout my life.

–  –  –

ACKNOWLEDGMENTS

LIST OF TABLES

LIST OF FIGURES

Abstract

CHAPTER 1 INTRODUCTION

2 EFFECTS OF CHRONIC METHYLMERCURY EXPOSURE ON PAIRING

BEHAVIOR AND REPRODUCTIVE SUCCESS OF THE WHITE IBIS

Introduction

Methods

Experimental Setup

Exposure of Captive Birds to Dietary Methylmercury

Behavioral Sampling during Breeding

Statistical Analyses

Results

Sex Ratio and Mercury Levels

Pair Formation and Nesting Success

Clutch Size, Hatchability and Fledging Success

Discussion

Homosexual Pairing and Reproductive Success

Clutch Size, Hatchability and Fledging Success

Conclusions

3 EFFECTS OF CHRONIC METHYLMERCURY EXPOSURE ON COURTSHIP

AND PARENTAL BEHAVIOR OF WHITE IBISES

Introduction

Methods

Experimental Setup and Dietary Methylmercury Exposure of White Ibises...... 60 Behavioral Sampling during the Breeding Season

Provision of breeding material and nest checks

Courtship behavior

Incubation behavior

Statistical Analyses

Results

Nest Initiations and Courtship Behavior

Parental Behavior

6 Discussion

Nest Initiations and Courtship Behavior

Parental Behavior

Conclusions

4 EFFECTS OF CHRONIC METHYLMERCURY EXPOSURE ON SEX

STEROIDS OF WHITE IBISES DURING THE BREEDING SEASON

Introduction

Methods

Dietary Methylmercury Exposure of Captive White Ibises

Behavioral Sampling during the Breeding Season

Collection of Fecal Samples

Radioimmunoassays for Steroid Hormone Metabolites in Fecal Extracts........ 91 Statistical Analyses of Hormone Data

Results

Reproductive Behavior

Effects of Methylmercury on Estradiol in Adult Females

Effects of Methylmercury on Estradiol in Adult Males

Effects of Methylmercury on Testosterone in Adult Females

Effects of Methylmercury on Testosterone in Adult Males

Discussion





Effects of Methylmercury on Sex Steroids

Homosexual Pairing and Endocrine Disruption of Sex Steroids in Males....... 103 Reproductive Success and Endocrine Disruption in Females

Dose-response Relationships between Methylmercury and Endocrine Disruption

Conclusions

5 EFFECTS OF CHRONIC METHYLMERCURY EXPOSURE ON

CORTICOSTERONE RESPONSES OF WHITE IBISES DURING

REPRODUCTION

Introduction

Methods

Experimental Setup and Exposure of Captive White Ibises to Methylmercury

Monitoring Breeding Behavior

Experimental Reduction of Food Availability during Breeding

Collection of Fecal Samples

Radioimmunoassays for Corticosterone Metabolites in Fecal Extracts.......... 133 Statistical Analyses

Results

Effects of Methylmercury and Food Stress on Corticosterone in Adult Females

Effects of Methylmercury and Food Stress on Corticosterone in Adult Males 136 Discussion

7 Effects of Methylmercury on Corticosterone during Reproduction.................. 138 Effects of Methylmercury and Food Stress on Corticosterone

Effects of Methylmercury on Corticosterone in Homosexually-paired Males.. 141 Conclusions

6 CONCLUSION

Introduction

Synthesis

Male-male Pairing in Ibises Induced by Methylmercury Exposure................. 155 Effects of Methylmercury on Reproduction in Females

Effects of Methylmercury on White Ibis Populations

Conclusions

APPENDIX A MEAN REPRODUCTIVE PARAMETERS

B FECAL CONCENTRATIONS OF ESTRADIOL AND TESTOSTERONE

METABOLITES IN WHITE IBISES

C FECAL CONCENTRATIONS OF CORTICOSTERONE METABOLITES IN

WHITE IBISES

LIST OF REFERENCES

BIOGRAPHICAL SKETCH

–  –  –

Results of chi-square (Χ2) tests testing deviance of sex ratios from one, in 2-1 each treatment group and year

2-2 Total mercury levels in feathers and blood for each treatment group................. 47 2-3 Results of linear models testing nest initiation dates of heterosexual and homosexual males in each treatment group in each year

Results of chi-square (Χ2) tests for proportions of homosexual and 2-4 heterosexual pair-days.

2-5 Percentage of females potentially excluded from breeding in free-living colonies due to male-male pairing.

2-6 Results of Kruskal-Wallis tests for treatment effects on clutch sizes, hatchability and fledging rates.

2-7 Means and standard errors (S.E.) of young fledged per female over three breeding attempts and the number of successful attempts over the same period..

3-1 Model results for number of head-bobs per observation session by treatment group in 2007

3-2 Model results for average number of head-bobs per male per observation session by treatment and pairing type in 2008.

3-3 Model results for number of pair-bows per observation session by treatment group in 2007

3-4 Model results for average number of pair-bows per pair per observation session by treatment and pairing type in 2008.

3-5 Model results for number of aggressive acts per observation session by treatment group in 2007.

3-6 Model results for average number of aggressive acts per male per observation session by treatment and pairing type in 2008.

3-7 Model results for average number of approaches by females per displaying male per observation session by treatment and pairing type in 2008................. 75 3-8 Model results for average number of approaches by males per displaying male per observation session by pairing type in 2008.

9 3-9 Model summaries for proportion of time spent at nest per observation session during the incubation stage, by sex and treatment group in 2007 and 2008.

4-1 Model summaries of the best models explaining estradiol concentrations in white ibis females.

4-2 Model summaries of the best models explaining estradiol concentrations in white ibis males.

4-3 Coefficients for each MeHg-dosed group comparing estradiol concentrations in each breeding stage relative to control males

4-4 Model summaries of the best models explaining testosterone concentrations in white ibis females.

4-5 Model summaries of the best models explaining testosterone concentrations in white ibis males.

5-1 Model summaries of the best models explaining corticosterone concentrations in white ibis females.

5-2 Coefficients comparing each dosed group with control females during each breeding stage in 2008.

5-3 Model summaries of the best models explaining corticosterone concentrations in white ibis males.

5-4 Coefficients comparing each dosed group with control males during each breeding stage in 2008

5-5 Coefficients comparing homosexual males in each dosed group with heterosexual males within the same group, by breeding stage in 2008........... 146 5-6 Coefficients comparing dosed males with control males during the period of food restriction in 2008.

6-1 Estimated reduction in reproductive output of dosed birds due to male-male pairing (unproductive nesting) and decreased fledgling production in females in comparison to the control group.

A-1 Mean clutch sizes, hatchability rates and fledging rates for each treatment..... 168 B-1 Mean and standard errors (S.E.) of fecal estradiol metabolites in female ibises in the first breeding attempt, 2007 for each treatment group and breeding stage.

10 B-2 Mean and standard errors (S.E.) of fecal estradiol metabolites in female ibises in the second breeding attempt, 2007 for each treatment group and breeding stage.

B-3 Mean and standard errors (S.E.) of fecal estradiol metabolites in female ibises in the first breeding attempt, 2008 for each treatment group and breeding stage.

B-4 Mean and standard errors (S.E.) of fecal estradiol metabolites in male ibises in the first breeding attempt, 2007 for each treatment group and breeding stage.

B-5 Mean and standard errors (S.E.) of fecal estradiol metabolites in male ibises in the second breeding attempt, 2007 for each treatment group and breeding stage.

B-6 Mean and standard errors (S.E.) of fecal estradiol metabolites in male ibises in the first breeding attempt, 2008 for each treatment group and breeding stage.

B-7 Mean and standard errors (S.E.) of fecal testosterone metabolites in female ibises in the first breeding attempt, 2007 for each treatment group and breeding stage.

B-8 Mean and standard errors (S.E.) of fecal testosterone metabolites in female ibises in the second breeding attempt, 2007 for each treatment group and breeding stage.

B-9 Mean and standard errors (S.E.) of fecal testosterone metabolites in female ibises in the first breeding attempt, 2008 for each treatment group and breeding stage.

B-10 Mean and standard errors (S.E.) of fecal testosterone metabolites in male ibises in the first breeding attempt, 2007 for each treatment group and breeding stage.

B-11 Mean and standard errors (S.E.) of fecal testosterone metabolites in male ibises in the second breeding attempt, 2007 for each treatment group and breeding stage.

B-12 Mean and standard errors (S.E.) of fecal testosterone metabolites in male ibises in the first breeding attempt, 2008 for each treatment group and breeding stage.

C-1 Mean and standard errors (S.E.) of fecal corticosterone metabolites in female ibises in the first breeding attempt, 2007 for each treatment group and breeding stage.

11 C-2 Mean and standard errors (S.E.) of fecal corticosterone metabolites in female ibises in the second breeding attempt, 2007 for each treatment group and breeding stage.

C-3 Mean and standard errors (S.E.) of fecal corticosterone metabolites in female ibises in the first breeding attempt, 2008 for each treatment group and breeding stage.

C-4 Mean and standard errors (S.E.) of fecal corticosterone metabolites in female ibises during the period of food restriction, 2008 for each treatment group and breeding stage.

C-5 Mean and standard errors (S.E.) of fecal corticosterone metabolites in male ibises in the first breeding attempt, 2007 for each treatment group and breeding stage.

C-6 Mean and standard errors (S.E.) of fecal corticosterone metabolites in male ibises in the second breeding attempt, 2007 for each treatment group and breeding stage.

C-7 Mean and standard errors (S.E.) of fecal corticosterone metabolites in male ibises in the first breeding attempt, 2008 for each treatment group and breeding stage.

C-8 Mean and standard errors (S.E.) of fecal corticosterone metabolites in male ibises during the period of food restriction, 2008 for each treatment group and breeding stage.

–  –  –

2-1 The male: female ratio of birds in each treatment group in each year................ 50 2-2 The mean and standard deviation of total feather mercury in each treatment group for each year.

2-3 Mean and standard deviation of blood mercury levels in 2008 for each treatment group.



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