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Leontin Balanean Fall 2010 University of Alberta Effects of acanthocephalan parasites on colour and carotenoid quantities of their intermediate host Gammarus lacustris in the context of variable lake productivity by Leontin Balanean A thesis submitted to the Faculty of Graduate Studies and Research in partial fulfillment of the requirements for the degree of Master of Science in Ecology Department of Biological Sciences ©Leontin Balanean Fall 2010 Edmonton, Alberta Permission is hereby granted to the University of Alberta Libraries to reproduce single copies of this thesis and to lend or sell such copies for private, scholarly or scientific research purposes only. Where the thesis is converted to, or otherwise made available in digital form, the University of Alberta will advise potential users of the thesis of these terms. The author reserves all other publication and other rights in association with the copyright in the thesis and, except as herein before provided, neither the thesis nor any substantial portion thereof may be printed or otherwise reproduced in any material form whatsoever without the author's prior written permission. Examining Committee Heather Proctor, Biological Sciences (supervisor) Rolf Vinebrooke, Biological Sciences (co-supervisor) Allen Shostak, Biological Sciences (supervisory committee member) Marianne Douglas, Earth and Atmospheric Science (examining committee member) David Coltman, Biological Sciences (chair of exam) Dedication To my wife Ana and her dog Laica, who courageously protected us from wild ‘beasts’ in the field and let me name one of the studied lakes after her. Abstract I studied the effects of Polymorphus paradoxus Connell and Corner and Polymorphus marilis Van Cleave on colour and carotenoid quantities of their host amphipod Gammarus lacustris G.O. Sars in seven lakes in Alberta, Canada, that differed in productivity. Polymorphus marilis induced ‘pigmentation dystrophy’ and a higher degree of blueness in both amphipod sexes than did P. paradoxus. Colour shifted toward lighter, bluer and greener tones, denoting less carotenoids, in amphipods parasitized by P. marilis. This is the first study to measure host- colour changes induced by parasites using consistent, repeatable digital analysis. Maximum carotenoid quantities were reached in hypereutrophic lakes where parasite-induced colour changes were also generally minimal. I developed regression models that accurately predict carotenoid quantities in amphipods by their colour, parasite status and water chemistry. This is the first study showing that carotenoid quantities and parasite-induced colour change in crustaceans depend on lake productivity. Aknowledgement I offer my deepest gratitude to my supervisor Heather Proctor for her constant moral and financial support, for her expertise and ideas that made this project possible. I also thank my co-supervisor Rolf Vinebrooke for his financial support, advice and expertise in analyzing carotenoids, and Al Shostak for his advice and expertise in identification of parasites. My thanks go also to Erin Bayne for his advice and time offered for channeling through advanced statistics, to Jon Johansson (Computer Sciences) for his advice and help in image analysis and to Jocelyn Hudon (Royal Alberta Museum) for his help in carotenoid identification. Thank you Charlene Nielsen for your help in constructing the map of sampled lakes. I would also like to thank my lab colleagues Bronwyn Williams and Jeffrey Newton who kindly and unconditionally offered their support. Thank you, Ana for the unlimited time you spent with me on the field and for your constant support. Table of Contents Chapter 1 - Introduction 1.1 Life cycle of Polymorphus paradoxus and P. marilis 1 1.2 Manipulative parasites – an overview 2 1.3 Colour, a phenotypic trait ‘manipulated’ by parasites 3 1.4 Parasite induced modifications in colour, linked to carotenoid composition 5 1.5 Parasite induced modifications in carotenoid composition 6 1.6 Parasite effect on carotenoids, more than a ‘pigmentation dystrophy’ issue 7 1.7 Environment–carotenoid interaction 8 1.8 Objectives 8 Literature cited 10 Chapter 2 - Acanthocephalan parasites, water quality and diet affect colour of the amphipod Gammarus lacustris 2.1 Introduction 16 2.2 Materials and methods 21 2.3 Results 29 2.4 Discussion 41 Literature cited 68 Chapter 3 - Effects of acanthocephalan parasites on carotenoid composition and body weight of Gammarus lacustris and a proposed carotenoid-colour relationship 3.1 Introduction 76 3.2 Materials and methods 83 3.3 Results 89 3.4 Discussion 100 Literature cited 117 Chapter 4 - General Discussion 4.1 Colour, carotenoids and influence of acanthocephalans on male and female hosts 124 4.2 Effect of diet and water chemistry on parasite-induced changes in colour, carotenoid quantities and weight 125 4.3 Concluding remarks 127 Literature cited 129 List of Tables Table 2-1. Chemical, physical and biological characteristics of the seven sampled lakes from Alberta, Canada 46 Table 2-2. Measurements of Polymorphus paradoxus and P. marilis everted cystacanths. The specimens were collected from Laica, Kettle, Range Road 223 and Beyette lakes, Alberta 46 Table 2-3. Colour differences between female and male G. lacustris when both are parasitized by P. paradoxus or P. marilis, or non-parasitized in seven lakes from Alberta. The colour differences ΔL*, Δa*, Δb* and ΔEab are calculated using equation 1-4 (Introduction) on the averages displayed by SPSS GLM descriptive statistics, using the colour of males as the standard colour 47 Table 2-4. Test of between-subjects effects (similar to ANOVA) showing the effect of variable ‘sex’ on the CIE L*, a*, b* vectors within a group, non-parasitized G. lacustris, parasitized by P. paradoxus and parasitized by P. marilis. α < 0.05. * indicates a significant difference 48 Table 2-5. CIE L*a*b* average values ± SD for scanned pictures of G. lacustris females and males from seven lakes from Alberta based on SPSS GLM output. α < 0.05 49 Table 2-6. Average CIE L*a*b* results for scanned pictures of parasitized and non-parasitized G. lacustris males in seven lakes from Alberta. p value, F test value and degrees of freedom are based on the General Linear Model (α <0.05) output in SPSS. P0= non-parasitized G. lacustris, P1= G. lacustris parasitized by P. paradoxus and P2= G. lacustris parasitized by P. marilis 50 Table 2-7. Test of between-subjects effects (ANOVA) showing the effect of the two species of parasites, P. paradoxus and P. marilis on the CIE L*, a*, b* colour vectors of parasitized amphipods when compared to non- parasitized ones within a sex group; α < 0.05. * indicates a significant difference 51 Table 2-8. Colour differences in G. lacustris males infected by P. paradoxus and P. marilis cystacanths when compared to non-parasitized males. ΔL*, Δa*, Δb* and ΔEab are calculated based on the L*, a* and b* averages displayed by the SPSS GLM analysis descriptive statistics for each group of amphipods, non-parasitized, P. paradoxus and P. marilis parasitized, and using the equations 1-4 (Introduction). P0= no. of non- parasitized G. lacustris, P1= no. of G. lacustris parasitized by P. paradoxus and P2= no. of G. lacustris parasitized by P. marilis 52 Table 2-9. Colour differences in G. lacustris females infected by P. paradoxus and P. marilis cystacanths when compared to non-parasitized females. ΔL*, Δa*, Δb* and ΔEab are calculated based on the L*, a* and b* averages displayed by the SPSS GLM analysis descriptive statistics for each group of amphipods, non-parasitized, P. paradoxus and P. marilis parasitized, and using the equations 1-4. P0=no. of non-parasitized G. lacustris, P1= no. of G. lacustris parasitized by P. paradoxus and P2= no. of G. lacustris parasitized by P. marilis 53 Table 2-10. Average CIE L*a*b* results for scanned pictures of parasitized and non-parasitized G. lacustris females in six lakes from Alberta. Significance p value, F test value and degrees of freedom are based on the General Linear Model output in SPSS (α <0.05). P0= non-parasitized G. lacustris, P1= G. lacustris parasitized by P. paradoxus and P2= G. lacustris parasitized by P. marilis; ‘-‘no data available 54 Table 2-11. Correlation between amounts of colour differences induced by P. paradoxus and P. marilis in amphipods and total phosphorus (TP) and dissolved organic carbon (DOC) from the sampled lakes 55 Table 2-12. Average ± SD values of CIE L*, a*, b* 1931 colour space of images of non-parasitized juvenile G. lacustris from Kettle Lake before entering the laboratory experiment. Values are obtained from the descriptive statistic of GLM in SPSS. α < 0.05 55 Table 2-13. PATN ANOSIM p-values for the colour differences in amphipods from 8 jars receiving 2 water treatments (WK and WN) and 2 food treatments (DK and DN). p-values for the pair-wise test between jars receiving the same water and food treatments are highlighted in grey. The cut-off for significance is 0.05 (SSH, MDS, Gower-Metric, Stress = 0.084 in 2 dimensions. WN,DN – water and diet from Narrow Lake; WK,DK – water and diet from Kettle Lake; WN,DK and WK, DN – combinations of water and diet from Narrow and Kettle lakes 56 Table 2-14. Average CIE L*, a*, b* values for amphipods under treatments of water (WN) and diet (DN) from Narrow Lake and water (WK) and diet (DK) from Kettle Lake. GLM output for testing the effect of different diets under similar water conditions and of the effect of different water under similar diet treatment is presented. α < 0.05 56 Table 2-15. The colour differences produced by treatments of diet (D) and water (W) from the oligotrophic Narrow Lake (DN and WN) and the hypereutrophic Kettle Lake (DK and WK) on the colour of G. lacustris juveniles. Differences in colour vectors and distance between two colours were calculated based on equation 1-4 (Introduction) and on the descriptive statistic output of GLM analysis in SPSS at α < 0.05 (Table 12).
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