Influence of feeding ecology on mercury accumulation in turtles and

111 Pages·2013·1 MB·English

Influence of feeding ecology on mercury accumulation in turtles and fish of the Rideau Canal, Ontario,
Canada.

Julie Châteauvert

Thesis submitted to the
Faculty of Graduate and Postdoctoral Studies
University of Ottawa
In partial fulfillment of the requirements for the
M.Sc. degree in the
Ottawa-Carleton Institute of Biology

Thèse soumise à la
Faculté des études supérieures et postdoctorales
Université d’Ottawa
En vue de l’obtention de la maîtrise ès sciences
Institut de biologie d’Ottawa-Carleton

© Julie Châteauvert, Ottawa, Canada, 2013
ABSTRACT

Pollution is a major cause of biodiversity declines worldwide. Therefore,
understanding exposure and uptake mechanisms for contaminants such as mercury (Hg) is
a crucial step in our efforts to understand the causes of species decline. I investigated the
influence of dietary reliance on the benthic food chain, and the influence of the proportion
of zebra mussels in the diet, on the accumulation of Hg in freshwater fish and turtle species.
I collected turtle blood samples and fish muscle samples in 2012 and analyzed these tissue
samples for carbon and nitrogen isotope ratios (δ13C and δ15N), and for Hg concentrations.
Isotopic ratios were used to calculate trophic level, dietary reliance on the benthic food
chain, and the proportion of zebra mussels in the diet. Reliance on the benthic food chain
was a good predictor of Hg concentration in fish muscle, but not in turtle blood. The
proportion of zebra mussels in the diet was not a good predictor of Hg in turtles or in fish.
My results indicate that dietary reliance on the benthos should be considered in future
tissue Hg modelling studies for fish, and that this predictor variable could be used to
identify other fish species likely to be burdened by high concentrations of Hg.

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RÉSUMÉ

La pollution est une des causes principales du déclin de la biodiversité dans le
monde. Par conséquent, une bonne compréhension des mécanismes d'exposition et
d'absorption des contaminants tels que le mercure (Hg) est une étape importante dans nos
efforts pour comprendre la hausse du taux d’extinction associée à la pollution. J'ai étudié
l'influence de la dépendance de la diète à la chaîne alimentaire benthique, et l'influence de
la proportion de moules zébrées dans la diète, sur l'accumulation de Hg chez les poissons et
les tortues d’eau douce. J'ai recueilli des échantillons de sang de tortue et de muscle de
poisson en 2012. J’ai ensuite analysé ces échantillons de tissus pour obtenir les ratios
d'isotopes d'azote et de carbone (δ13C et δ15N) et la concentration de Hg. J’ai utilisé les
ratios isotopiques pour calculer le niveau trophique, la dépendance de la diète à la chaîne
alimentaire benthique et la proportion des moules zébrées dans la diète. Mes résultats
démontrent que la dépendance de la diète à la chaîne alimentaire benthique est un bon
prédicteur de la concentration de Hg dans le muscle de poisson, mais pas dans le sang de
tortue. La proportion des moules zébrées dans la diète n'était pas un bon prédicteur de la
concentration en Hg chez les tortues ou les poissons. Mes résultats indiquent que la
dépendance alimentaire sur le benthos est une variable qui devrait être considérée dans les
études futures de modélisation chez les poissons. De plus, cette variable pourrait être
utilisée pour identifier les espèces de poissons susceptibles d'être affectés par des
concentrations élevées de Hg.

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ACKNOWLEDGEMENTS

I would like to express my deepest appreciation to all those who provided me the
possibility to complete this thesis. First and foremost, I would like to thank my supervisor,
Gabriel Blouin-Demers, for providing me with the opportunity to work on this applied
conservation project. Gab, you were always available to answer questions and to guide my
learning process. You answered all my emails with incredible speed, and you always
provided the most pertinent and useful information. Grégory Bulté, one of Gab’s previous
graduate students and now an Instructor at Carleton University, is also one of the first
people I would like to thank. Having worked on similar projects in the past, Greg was not
only able to provide timely feedback on every draft of my thesis, but also to suggest the
best and most current methods to use in the field, in the laboratory, and in my statistical
analyses. Once again, thank you.
I would also like to thank Parks Canada for funding the project, for providing me
with field assistants, and for lending me their boat. Morgan Brown, Rachel Mayberry, and
Shannon Moore spent hours trying to make the fishing gear I requested by hand… That’s
dedication! Hillary Knack and Chantal Vis always made sure that I had everything I needed
to complete my field work and they provided valuable feedback every step of the way.
Thank you all for the opportunity to work with you on this project.
My sincere acknowledgements to the official and unofficial members of my
committee: Grégory Bulté, Alexandre Poulain, Frances Pick, and Linda Campbell. Thank you
for sharing your professional expertise, and for reviewing every document I produced,
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including seminar presentations, reports to Parks Canada, and thesis-related documents.
Together, you were able to answer every question I could come up with, as well as the
questions I hadn’t even thought of asking!
To everyone at QUBS, thank you for making my field work the most enjoyable
experience possible. In particular, I want to thank Veronica Jaspers-Fayer for making the
best food I have ever eaten, and Frank Phelan and Mark Conboy for providing me with all
the tools and knowledge necessary to be successful in the field.
I am also lucky to have had such amazing colleagues in the herpetology lab,
including Gabrielle Fortin, Victor Thomasson, Rayan El Balaa, William Halliday, Lauren Stoot,
Nick Cairns, and Véronique Juneau. Véro, thank you for letting me come over to your house
every day of the week for three months to work on my thesis and for keeping me on task
during the final writing phase of my thesis project. Nick and Lauren, thank you for teaching
me how to catch turtles! I also want to thank my field assistants Morgan Brown, Guillaume
Slevan-Tremblay, Chad Stewart, and Morgan Salaun-Miller. None of this would have been
possible without your hard work and dedication in the field and in the lab.
Finally, I want to thank my best friend Deirdre Trudeau, and my mother Chantal
Boudreault, who both read everything I wrote during the last two years to correct my
spelling and grammar mistakes. I should also thank all my friends and my whole family for
listening to me talk on and on about how awesome I think turtles are, and about how much
I love science. Even though this project is nearing completion, I may never stop dropping
random turtle facts in our everyday conversations!
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TABLE OF CONTENTS

ABSTRACT ............................................................................................................................................... ii
RÉSUMÉ ................................................................................................................................................. iii
ACKNOWLEDGEMENTS .......................................................................................................................... iv
TABLE OF CONTENTS ............................................................................................................................. vi
LIST OF TABLES ...................................................................................................................................... ix
LIST OF FIGURES ................................................................................................................................... xii
GENERAL INTRODUCTION ..................................................................................................................... 1
CHAPTER 1: Dietary reliance on the benthic food chain influences mercury accumulation in
freshwater turtles and fish .................................................................................................................. 12
ABSTRACT ........................................................................................................................................ 13
INTRODUCTION................................................................................................................................ 14
METHODOLOGY ............................................................................................................................... 17
Study area .................................................................................................................................... 17
Turtle capture .............................................................................................................................. 17
Fish capture ................................................................................................................................. 18
Blood sampling ............................................................................................................................ 18
Fish muscle sampling ................................................................................................................... 19
Prey species sampling .................................................................................................................. 19
Mercury analyses ......................................................................................................................... 20
Total Mercury .......................................................................................................................... 21
Methylmercury ........................................................................................................................ 21
Carbon and Nitrogen Isotope Ratios ........................................................................................... 22
Trophic Level and Reliance on the Benthos................................................................................. 23
Modeling ...................................................................................................................................... 23
RESULTS ........................................................................................................................................... 25
Turtles .......................................................................................................................................... 25
Model Variables ....................................................................................................................... 25
Modeling and Validation ......................................................................................................... 26
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Cross-Validation ....................................................................................................................... 26
Fish .............................................................................................................................................. 27
Model variables ....................................................................................................................... 27
Modeling and Validation ......................................................................................................... 28
Cross-Validation ....................................................................................................................... 28
DISCUSSION ..................................................................................................................................... 29
Turtles .......................................................................................................................................... 31
Fish ............................................................................................................................................... 33
Applications and future modeling exercises ............................................................................... 35
CHAPTER 2: The proportion of zebra mussels (Dreissena polymorpha) in the diet of musk turtles
(Sternotherus odoratus) and pumpkinseeds (Lepomis gibbosus) does not influence the accumulation
of mercury ........................................................................................................................................... 46
ABSTRACT ........................................................................................................................................ 47
INTRODUCTION................................................................................................................................ 48
METHODOLOGY ............................................................................................................................... 53
Study area .................................................................................................................................... 53
Turtle and fish capture ................................................................................................................ 53
Blood sampling ............................................................................................................................ 54
Fish muscle sampling ................................................................................................................... 54
Prey species sampling .................................................................................................................. 55
Mercury analyses ......................................................................................................................... 56
Total Mercury .......................................................................................................................... 56
Methylmercury ........................................................................................................................ 56
Carbon and Nitrogen Isotope Ratios ........................................................................................... 57
Trophic Level ................................................................................................................................ 58
Proportion of zebra mussels in the diet ...................................................................................... 58
Modeling ...................................................................................................................................... 59
RESULTS ........................................................................................................................................... 60
Modeling and Validation ............................................................................................................. 61
DISCUSSION ..................................................................................................................................... 63
General Conclusion .............................................................................................................................. 72
APPENDIX I ........................................................................................................................................... 75
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THg Concentration as a Measure of MeHg Concentration ............................................................. 76
Collinearity ....................................................................................................................................... 76
Candidate models ............................................................................................................................ 77
APPENDIX II .......................................................................................................................................... 84
THg Concentration as a Measure of MeHg Concentration ............................................................. 85
Collinearity ....................................................................................................................................... 85
Candidate models ............................................................................................................................ 86
Snails and filter-feeding ................................................................................................................... 86
Literature Cited .................................................................................................................................... 91

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LIST OF TABLES

Table 1 – 1. Variability in measurements of the predictors used in modeling THg
concentrations in turtles (n = 99) and in fish (n = 119). Size of the animals is indicated in
centimeters (cm) and PSNAIL is a proportion. Trophic level (TL) was calculated using the
formula described in Post et al. (2002). All measurements are given as average (M) ±
standard error (SE) (minimum – maximum).
Table 1 – 2. Averaged parameter coefficients for two logistic regression models predicting
THg concentrations in A. turtles (n = 99) and B. fish (n = 119). Standard error (SE) and
95% confidence intervals (95% CI) are given for each parameter.
Table 1 – 3. Predictive ability assessment for 16 averaged models predicting turtle and fish
tissue THg concentration on internal data (n = 19 – 30). Coefficient of determination
(R2), p-value (p), and slope (m) and intercept (b) of the linear fit between observed
(OBS) and predicted (PRE) THg concentrations (ng/g) are presented. The name of the
training set refers to the data that was taken out of the full data set to create the
testing set.
Table 1 – 4. Parameter coefficients for eight averaged multiple linear regression models
predicting THg for A. turtles (n = 19 – 20) and B. fish (n = 19 – 30). The number of the
study site S1 – S4, and the number of the random sub-samples R1 – R4 refer to the data
excluded from each training set to create the testing set. The z-score of the coefficients
highlighted in grey were not significant.
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Table 2 – 1. Variability in measurements of the predictors used in modeling THg
concentrations in musk turtles (n = 39) and in pumpkinseeds (n = 20). Size of the
animals is indicated in centimeters (cm) and PZEBRA is a proportion. Trophic level (TL)
was calculated using the formula described in Post et al. (2002). All measurements are
given as an average ± standard error (SE) (min – max).
Table 2 – 2. Relative importance of each predictor variable in the averaged model for A.
musk turtles and B. pumpkinseeds.
Table 2 – 3. Averaged parameter coefficients for two logistic regression models predicting
THg concentrations in A. musk turtles (n = 39) and B. pumpkinseeds (n = 20). Standard
error (SE), z-scores, p-values, and 95% confidence intervals (95% CI) are given for each
parameter.
Table 2 – 4. Slope (m) and y-intercept (b) for the regression between observed and
predicted THg concentrations, along with the 95% confidence intervals (95% CI) are
given for the musk turtle and pumpkinseed models. R2, RMSD, U , U , and U
error slope error
are also given.
Table A1-1. Candidate multiple linear regression models predicting THg concentrations in A.
turtles (n = 99) and B. fish (n = 119) for the full data set. Models are ranked by
increasing order of second order Akaike Information Criterion (AICc and ΔAICc < 4). The
number of parameters (k), as well as the Akaike weights (w), are listed.
x