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Respiratory Plasticity in the Amphibious Fish, Kryptolebias Marmoratus During Emersion

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Respiratory Plasticity in the Amphibious Fish, Kryptolebias Marmoratus During Emersion Respiratory plasticity in the amphibious fish, Kryptolebias marmoratus during emersion by Tessa Blanchard A Thesis presented to The University of Guelph In partial fulfilment of requirements for the degree of Master of Science in Integrative Biology Guelph, Ontario, Canada © Tessa Blanchard, December, 2017 ABSTRACT Respiratory plasticity in the amphibious fish, Kryptolebias marmoratus during emersion Tessa Blanchard Advisor: University of Guelph, 2017 Dr. Patricia Wright Amphibious fishes have evolved multiple adaptive strategies for respiring out of water. I tested the hypothesis that in amphibious fish that leave water, enhanced respiratory performance on land is the result of rapid functional phenotypic flexibility of respiratory traits. Initially, K. marmoratus had improved respiratory performance (lower aerial critical oxygen tension (Pcrit), higher regulation index (RI)) after only 1 day of air exposure. Initial changes in aerial Pcrit were strongly associated with the relative change in hematocrit. Also, initial changes in RI were highly linked to increased dorsal cutaneous angiogenesis. Long-term changes (7 days) in respiratory traits were not significantly linked to the variation in either aerial Pcrit and RI. Overall, two phases were involved in the enhancement of aerial respiration; an initial rapid response and a delayed response. My findings suggest that the initial rapid response is due to flexibility in both O2-uptake and O2- carrying capacity. iii Acknowledgments First and foremost, I would like to sincerely thank my wonderful supervisor Dr. Patricia Wright. Pat, thank you for being an amazing mentor, for your endless support throughout this journey and for always steering me in the right direction. You are an inspiration to women in science and I am truly thankful I had the opportunity to learn from such an incredible researcher. I am more thankful than words can express. I would like to extend thanks to my committee members Dr. Nick Bernier; for always having your door open when I needed advice and Dr. Beren Robinson; for your expertise and guidance with statistical analysis. Thank you to Matt Cornish and Mike Davies for your expertise and equipment from the Aqualab. I personally would like to thank Andy Turko for his contributions to my thesis. Your innovative ideas and creative-DIY-engineering designs in respirometry made this project possible. You have inspired me to be a better scientist and for that I will always be grateful. I would like the sincerely thank all the wonderful people I have met throughout these past two years: Elizabeth T., Giulia R., Hailey A., Hailey H., Lauren G., Kelly L., Robyn S., Sarah B. and Sarah S. You guys were like family and my time at Guelph wouldn’t have been the same without you guys. Finally, I would like to thank my parents Carole and Rach, Ian and Christine for all your love and support during these past two years. Thank you all. iv Table of Contents Abstract…………………………………………………………………………………………....ii Acknowledgments…………...………………………………………………………………...…iii Table of Contents……………………………………………………………………………...….iv List of Figures……………………………………………………………………..…………..…..v List of Tables……………………………………………………………………..……………..viii Introduction…………………………………………………………………………………….….1 Methods…………………………………………………………………………………………..10 Results…………………………………………………………………………………………....18 Discussion…………………………………………………………………………………….….43 Literature Cited……………………………………………………………………………….….57 v List of Figures Figure 1 Preliminary oxygen consumption rate measurements of K. marmoratus in air over time. Data are presented as means ± SEM (N=8)………………….........p. 16 Figure 2 Aerial step-wise hypoxia protocol for amphibious fishes. Oxygen consumption was measured at a PO2 of 21.2kPa and then at a PO2 of 14.8kPa to 10.6kPa in steps of 2.1kPa and from 10.6kPa to 1.1kPa in steps of 1.1kPa. Data are presented as raw values from a single fish…………………………………………………...…..p. 17 Figure 3 Oxygen consumption rates in response to varying atmospheric oxygen levels in Florida (A), Honduras (B), Belize (C), and Freshwater (D) strains of K. marmoratus acclimated to air for 0, 1, 3 and 7 days. Data are presented as means ± SEM (N=8-16)...……………………………………….…………….………p. 22 Figure 4 Critical oxygen tension in air (aerial Pcrit) of four strains of K. marmoratus acclimated to air for 0, 1, 3 and 7 days. Data are presented as means ± SEM (N= 8-16). Different letters (upper-case) indicate statistically significant differences in Pcrit across time and different letters (lower-case; shown in legend) indicate statistically significant differences in Pcrit across strains, irrespective of time, as determined by a Two-Way ANOVA (P<0.05)…………………………...……p. 24 Figure 5 Critical oxygen tension in air (aerial Pcrit) of four strains of K. marmoratus acclimated to air for 0 and 7 days and were either fed or fasted for 7 days. Data are presented as means ± SEM (N=8-16). Groups that do not share the same letter are significantly different from each other as determined by a Two-Way ANOVA (P<0.05). Note: 0-Fed Water and 7-Fasted Air were presented in Figure 4…...p. 26 vi Figure 6 Regulation Index (RI) of four strains of K. marmoratus acclimated to air for 0, 1, 3 and 7 days. Data are presented as means ± SEM (N=8-16). Groups that do not share the same letter are significantly different as determined by a Two-Way ANOVA (P<0.05)……………….…………………………….………....……p. 28 Figure 7 Routine metabolic rate (O2 uptake) of four strains of K. marmoratus acclimated to air for 0, 1, 3 and 7 days. Data are presented as means ± SEM (N= 8-16). Groups not sharing the same letter are significantly different as determined by a Two-Way ANOVA (P<0.05). ……………………………..…………..…p. 30 Figure 8 Representative images of the angiogenesis marker, CD31 stained, dorsal and ventral epidermis of K. marmoratus acclimated to air for 0, 1, 3 and 7 days. A: Dorsal 0 days, B: Dorsal 1 day, C: Dorsal 3 days, D: Dorsal 7 days, E: Ventral 0 days, F: Ventral 1 day, G: Ventral 3 days, H: Ventral 7 days. Scale bar = 50 µm. E: Epidermis; D: Dermis; Arrowhead: Mucous cell……………..………………..p. 32 Figure 9 Expression of the angiogenesis marker CD31 within the dorsal (A) and ventral (B) region of the epidermis in four strains of K. marmoratus acclimated to air for 0, 1, 3 and 7 days. Data are presented as means ± SEM (N=6-8). Groups not sharing the same letter are significantly different as determined by a Two-Way ANOVA (P<0.05)………………...…………………………………………...p. 34 Figure 10 Relationship between relative change in RI and relative change in dorsal angiogenesis across four strains of K. marmoratus at 1 day (A: y = 0.90x - 0.08, P<0.01) and 3 days (B: y = 0.70x - 0.26, P<0.05) of air exposure. Data presented as mean values (N=8). Note: Data also presented in Table 1…………………..p. 36 vii Figure 11 Hematocrit (A) and number of red blood cells (B) for each of four strains of K. marmoratus acclimated to air for 0, 1 and 7 days. Data presented as means ± SEM (N=6-9). Strains not sharing the same letter are significantly different as determined by a Two-Way ANOVA and a posthoc Holm- Sidak test (P<0.05). An asterisk denotes significant differences within a strain from the 0-day value (Control).………………………………………………………………………p. 38 Figure 12 Relationship between relative change in aerial Pcrit and relative change in hematocrit at 1 day (y = 0.74x + 0.15, P=0.01) of air exposure in four strains of K. marmoratus. Data presented as mean values (N=8). Note: Data also presented in Table 1.……………………………………...…...……………………….…p. 40 viii List of Tables Table 1 Summary of univariate linear relationships between the relative change in respiratory performance (aerial Pcrit and RI) and the relative change in each respiratory trait across four strains of K. marmoratus acclimated to air for 1, 3 and 7 days. ……………………………………..……………………………p. 41 Table 2 Mean corpuscular volume (MCV) (fl) across four strains of K. marmoratus acclimated to air for 0, 1 and 7 days……………………………...……….…p. 42 Introduction Air-breathing in fishes is thought to have appeared during the late Devonian period, in response to aquatic hypoxia (Graham, 1997). There are two proposed categories of air-breathing fishes: amphibious fishes (leave water and breath air on land) and aquatic air-breathing fishes (gulp air at the interface of air and water) (Graham, 1997). My MSc thesis focused exclusively on amphibious fishes. Amphibious fishes are described as spending a portion of their life out of water (emersion) as part of their natural life history (Gordon et al., 1969). Emersion length varies between amphibious fishes: mudskippers (Periophthalmus sobrinus) can sustain around ~ 1½ days emersed (Gordon et al., 1969), mangrove rivulus (Kryptolebias marmoratus) can survive up to 2 months out of water (Taylor, 1990) and the lungfish (Protopterus aethiopicus) can survive years on land (Smith, 1931). However, the mechanisms responsible for differences in emersion tolerance across species are not clearly understood. One possibility is that emersion tolerance is related to their degree of respiratory plasticity. The transition from an aquatic to terrestrial environment imposes many physiological and environmental challenges for amphibious fishes (i.e. respiration, waste excretion, iono- and osmoregulation: Brown et al., 1992; Sayer, 2005). Therefore, amphibious fishes evolved mechanisms to maximize their fitness in water and air either through adaptive canalized or plastic traits (Graham, 1997). I am particularly interested in phenotypic plasticity and how this may affect performance out of water. Phenotypic plasticity is the result of a single genotype producing multiple phenotypes in response to environmental variation (West- Eberhard, 1989). I define plasticity as the expression of an alternative phenotype in response to a new environment (air exposure) compared to the aquatic phenotype. The goal of my MSc thesis was to understand whether the plasticity of different respiratory traits plays a functional role in respiration out of water in the amphibious fish Kryptolebias marmoratus.
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