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Feminization in Common Terns (Sterna Hirundo)

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Feminization in Common Terns (Sterna Hirundo) FEMINIZATION IN COMMON TERNS (STERNA HIRUNDO): RELATIONSHIP TO PERSISTENT ORGANIC CONTAMINANTS by Constance Ann Hart B. A. Chemistry College of St. Catherine, Saint Paul, MN 1989 SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY at the MASSACHUSETTS INSTITUTE OF TECHNOLOGY and the WOODS HOLE OCEANOGRAPHIC INSTITUTION January, 1998 © Constance A. Hart, 1998 All right reserved. The author hereby grants to M.I.T. and W.H.O.I. permission to reproduce and distribute copies of this thesis document in whole or in part. Signature of Author-=-=--=-"""--=~-=-----=-----------------­ Joint Program in Biological Oceanography Massachusetts Instit¥te of Technology/Woods Hole Oceanographic Institution Certified by--:;:-:;:-~--;:;:;:;---~::---'=--=--:---~--------------'--:--­ Mark E. Hahn, Thes.is Supervisor Accepted by Mark E.-::H-:;-a--;-h-n-,C:::::-ha--=i-r ------------=---------- Joint Committe for Biological Oceanography, Massachusetts Institute of Technology/Woods Hole Oceanographic Institution 2 This thesis is for my Dad, Tom Hart 3 4 FEMINIZATION IN COMMON TERNS (STERNA HIRUNDO): RELATIONSHIP TO PERSISTENT ORGANIC CONTAMINANTS by Constance Ann Hart submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy ABSTRACT Concern about skewed sex ratios and female-female pairings among endangered roseate terns (Sterna dougallii) on Bird Island in Buzzards Bay, Massachusetts prompted studies with common terns from the same site as a surrogate species. Over seventy percent (11115) of male common tern embryos sampled from this site in 1993 had testes containing areas of ovarian cortical tissue (ovotestes), suggesting that terns may be affected by endocrine-disrupting contaminants. These terns are exposed to non-ortho PCBs which bind to the aryl hydrocarbon receptor (AhR), and lower chlorinated PCBs, hydroxy­ metabolites of which bind to the estrogen receptor. Our objectives were to document the presence of ovotestes in common tern embryos from Bird Island and Nauset, a reference site, in 1994, and to determine the relationship between environmental contaminants and ovotestes development, as well as other health-related effects. Pipping tern embryo gonads were examined histologically, and yolk sacs were extracted and analyzed for PCBs and chlorinated pesticides. Extracts also were analyzed for dioxin equivalents (TCDD-EQs) using a chick embryo hepatocyte (CEH) bioassay. Total PCBs were significantly higher in Bird Island tern embryos (mean 114, range 17- 663 ugig lipid) than Nauset (mean 35, range 8- i 78 ugig lipid); but were variable at both sites. Total PCBs were highly correlated with TCDD-EQs. Tern hepatic EROD activity was relatively insensitive to induction; only when TCDD-EQs were above 82 ± 26 ng/g lipid were EROD activities elevated. Levels of organic pesticides were below levels thought to be of toxicological significance. The percentage of male tern embryos with ovotestes at Nauset (60%) and Bird Island (78%) was high and not significantly different; ovotestes in terns from both sites ranged in severity from absent (1) to intersex (4). There was no significant relationship between ovotestes severity and any of the contaminants measured. However, the data suggested a contaminant level threshold of 100 ug/g lipid total PCBs and 30 ng/g lipid TCDD-EQs above which the formation of ovotestes in tern embryos is more likely to occur. Principal component analysis of PCB isomer patterns distinguished between Bird Island and Nauset sites, with Bird Island having relatively higher levels of lower chlorinated PCBs; however, there was no distinction between terns with ovotestes and those without. Common tern prefledglings and paired same-nest eggs were collected from Bird Island in 1995 to examine the persistence of ovotestes. Gonadal histology revealed no ovarian tissue on testes, indicating that the ovotestes do not persist after 3 weeks posthatch. Our data suggested that: 1) ovotestes could be related to contaminants; 2) a background level of ovotestes may be present, but elevated by contaminant exposure; or 3) ovotestes could be normally present in male common tern embryos at hatching. Observations of the normal presence of persistent cortical tissue in the testes of several avian species suggest that concern about feminizing effects of contaminants on bird populations as measured by ovotestes development in hatching birds may be exaggerated. Before conclusions can be made about terns from Bird Island, it is necessary to establish whether persistent ovarian cortical areas in testes are normally present. Studies with common terns from a pristine site are currently underway. Thesis supervisor: Mark E. Hahn, Associate Scientist, WHOI 5 6 ACKNOWLEDGMENTS There are a great many people to whom I owe thanks for their continued involvement, support, and encouragement. First, I would like to thank my advisor Mark Hahn for his enthusiasm, patience, support, and abundance of literature. As Mark's first student, I believe we have both learned a lot over the years it has taken to complete this thesis, and it is a big accomplishment for us both. I have learned a great deal from the freedom Mark has allowed me, and have been able to develop confidence in myself through my own successes and failures. My committee members have also been a great help toward completion of this thesis. John Stegeman has always been ready with input at just the right moment, be it invaluable advice or a corny joke. Judy McDowell has always been available with positive advice and support. Pete Dedon (M.I.T.) has been extremely helpful both with advice and a willingness to accommodate Woods Hole students by travel or satellite link. I benefited greatly from spending nine months in the laboratory of Sean Kennedy (Canadian Wildlife Service), and thank him for being my mentor and friend. Finally, this work would not have been possible without Ian Nisbet who aiiowed me to become a part of this project. I have enjoyed every visit to Bird Island, and look forward to more. I would also like to thank Lauren Mullineaux for chairing my thesis defense, sharing the slidemaker with me, and helping to make the Jamaica trip very memorable. I also thank Larry Madin for chairing my thesis proposal defense and for somehow managing to fix one of the three non-working overhead projectors available. I owe great thanks to Michael Moore, who initially encouraged my involvement in this project. He, along with Ian Nisbet, Jeremy Hatch, and D. Michael Fry started the 1994 embryo collections, and I thank them all for their support. This project has required research in numerous disciplines, and thus, has been a continuing challenge from which I have learned a tremendous amount, including the importance of looking at the older literature. The gonadal histology on the 1994 pipping common tern embryos was carried out by D. Michael Fry at U.C. Davis. I thank both Michael Fry and Lela Preston (U.C. Davis) for completing this work and providing me with the data, as well as answering numerous questions. I would also like to thank Michelle McCafferty and Roxanne Smolowitz at the MBL for helping me to embed and section the prefledgling gonads. Michelle provided me with extremely high quality slides, and I thank her for all her help. Roxanne Smolowitz, 7 Michael Moore, D. Michael Fry, and Laird Shutt were all very helpful with interpretation and confirmation of gonadal histology. Much of this work was completed at the Canadian Wildlife Service in Hull, Quebec, where I spent nine very busy months in Sean Kennedy's laboratory. Sean and the members of his lab, Len Bastien, Stephanie Jones, and Angela Lorenzen, were invaluable for completing the egg and yolk sac extractions and the chick embryo hepatocyte bioassay. Also at CWS, Henry Won was extremely helpful and generous in carrying out the chemical analysis on my samples. Debbie Ashby taught me how to prepare my samples for chemical analysis, and Henry provided me with proper materials, carried out the injections, provided the analysis reports and helped with interpretations. Abde Idrissi also provided many insights and advice for all steps of the extractions. Also very helpful were Dr. Tony Scheuhammer and the members of his laboratory, Della Bond and Elyse Routhier, who carried out the mercury analysis on common tern embryo tissues. I also want to thank Dr. Laird Shutt, Glen Fox, Dr. Ross Norstrom, Brian Collins, Courtney Sandau, Rob Letcher, Masresha Asrat, and Karen Timm who provided helpful discussions and materials for this work. I would particularly like to thank Glen Fox who has continually shown interest in this work and provided insights and literature from his vast collection. I would also like to thank Dr. Laird Shutt along with Angela Lorenzen; their work on common terns from Canadian sites and willingness to collaborate has provided and will continue to provide interesting data and results. At WHOI, I want to thank all the members of Mark Hahn's lab who have provided daily help and support, including Bonnie Woodward, Sibel Karchner, Sue Bello, Brenda Jensen, Diana Franks, and Wade Powell. I am especially grateful for my long-time office mates and friends, Bonnie and Sibel who were always there to help, to listen, and to laugh with. I also want to thank all the members of John Stegeman's lab who have also been a great help on a daily basis, including Michael Moore, Bruce Woodin, Margie Oleksiak, Eli Hesterman, Jennifer Schlezinger, Rachael Cox, Carolyn Miller, Shannon Bard, Stefanie Valentini, Stephanie Innis, Celine Godard, Michael Morss, Heather Handley, Joanna Wilson, Malin Celander, and Renee White. Bruce has been especially helpful with teaching lab techniques, finding long lost supplies and equipment, and providing numerous concert diversions. Rachael Cox has been a big inspiration during the last few months of trying to complete this thesis, as she has been doing the same (while having a baby). I want to thank Michael Morss for all his help, especially with histology and dissections.
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