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In Angelfish Pterophyllum Scalare Ben-Gurion University of the Negev Jacob Blaustein Institutes for Desert Research Albert Katz International School for Desert studies Swimbladder non-inflation (SBN) in angelfish Pterophyllum scalare: Histological characterization and the role of environmental factors Thesis submitted in partial fulfillment of the requirements for the degree of "Master of Science" By: Shira T. Perlberg Under the Supervision of Dr. Dina Zilberg1 and Dr. Arik Diamant2 1Albert Katz Department of Dry Land Biotechnologies Ben- Gurion University of the Negev, Sde Boqer 2National Center for Mariculture Israel Oceanographic Limnological Research, Eilat Authors Signature…………………………………. Date………….. Approved by the Supervisors……………………… Date………….. Approved by the Director of the school………….. Date………….. Ben-Gurion University of the Negev Jacob Blaustein Institutes for Desert Research Albert Katz International School for Desert studies Swimbladder non-inflation (SBN) in angelfish Pterophyllum scalare: Histological characterization and the role of environmental factors Thesis submitted in partial fulfillment of the requirements for the degree of "Master of Science" By: Shira T. Perlberg March 2006 I Swimbladder non-inflation (SBN) in angelfish, Pterophyllum scalare: histological characterization and the role of environmental factors. By: Shira T. Perlberg This thesis is in partial fulfillment for the degree of Master of Science in Ben-Gurion University of the Negev, The Jacob Blaustein Institutes for Desert Research, Albert Katz international School for Desert Studies, 2006. Failure to inflate the swim bladder has been regarded a major obstacle in the rearing of many fish species. Recently, a large-scale phenomenon of swim bladder non-inflation (SBN) was reported in angelfish, Pterophyllum scalare, grown at a commercial ornamental fish farm in the Arava Valley, Israel (Zilberg et al. 2003). Failure to inflate the organ in the first two weeks post hatching resulted in swim bladder atrophy, dysfunctional buoyancy control, body deformities and decreased growth rates. A three- year survey was conducted in order to monitor SBN prevalence in the farm. The survey revealed no pattern for SBN occurrence in the farm and no relation to seasonality. To test the effect of environmental factors on SBN, eggs were hatched under different ambient conditions and larvae were examined under a light microscope for the presence of inflated swimbladders at 12 days post hatch (p.h.). Access to the air-water interface, feed concentration, delayed initiation of feeding (7th instead of 5th day p.h.), water conductivity (range of 110-1,015 μs) and tank coloration had no observable effect on SBN. Methylene Blue (MB), a fungicide routinely prophylactically employed to treat eggs, significantly increased the prevalence of SBN at a concentration of 5 ppm (28% II vs. 9% in the control). Methylene blue is suggested to have a teratogenic effect on angelfish larvae at these concentrations. For histological characterization, larvae were sampled at 0 to 12 days p.h.. During normal development, the primordial swimbladder was first discernable at the end of the 1st day p.h as a primordium of epithelial cells with a central lumen surrounded by a sheath of connective tissue. Initial inflation occurred on the 4th day p.h. before initiation of feeding (day 5). Prior to inflation, the swimbladder epithelium consisted of an internal layer of columnar cells and an external layer of squamous cells. The columnar epithelial cells were filled with an amorphous material of unknown nature in their basal region and their nuclei were situated apically. A pneumatic duct was not observed, suggesting that angelfish are physoclists. A primordial rete mirabile was present on the ventral part of the swimbladder, extending towards its posterior end. Upon inflation, the swimbladder epithelium transformed into a cuboidal to squamous form, as the lumen swelled with gas and the amorphous material disappeared. A model for the role of the amorphous material in normal inflation is suggested. Abnormal swimbladders were apparent from the 4th day post hatch. Three types of abnormalities were identified: 1) swimbladders with little or no amorphous material in the epithelial cells; 2) swimbladders with folded epithelium; 3) swimbladders with disorganization of the epithelium and little or no amorphous material. In larvae that failed to inflate their swimbladders after the 4th day, the epithelial cells proliferated in a disorganized manner and the uniform monolayer lost its regular appearance. Histologically, non-inflated swimbladders in fish hatched in 5 ppm MB were similar to abnormal swimbladders in fish raised under normal conditions (0.5 ppm Methylene blue). Understanding the way MB inhibits swimbladder inflation could shed light on SBN in angelfish. III Acknowledgement I would like to thank my supervisors Dr. Dina Zilberg and Dr. Arik Diamant for their moral support and professional guidance along the way. I couldn’t have picked better companions for this journey. I would also like to thank Dr. Rivka Ofir, for assisting with the more molecular point of view in the research. I would like to thank Shaul and Monik Hareel, Nitsan and Janta from “Negev Angels” fish farm, for their great work on the survey and wonderful cooperation. I hope this work will be useful for you in the future. I would like to thank Tamar Sinai, Shai Abutbul, Marcia Pimenta Leibovitz and Claudia Sanabria for all the help with the experiments in the lab in Sde boker, and the administrative staff of the school: Dorit Levin, Ilana Saller and Dina Fiengold for making things so much easier. A special thanks to all the people in the lab in Eilat: Barbara and Angelo Colorni, Sharon Ram, Gilaad Hienish and Asaf lipshitz for hosting me for 4.5 month and making me feel at home. Most of all, I would like to thank my amazing family, the Perlbergs: My father and mother- for helping me look at things in the right proportions and giving me so many advices. I have learned so much from you both. My brothers and sisters for always being there when I needed them. And finally, my grandmother- for inspiring me to pursue my own dreams. IV Table of contents Page Abstract…………………………………………………………………………….. I Acknowlegement…………………………………………………………………… III Table of contents…………………………………………………………………… IV List of tables………………………………………………………………………... V List of figures………………………………………………………………………. V 1. Introduction…………………………………………………………………... 1 1.1. Architecture and function of the adult teleost swimbladder………………….... 1 1.2. Initial swimbladder inflation…………………………………………………… 3 1.2.1. Mechanism of initial inflation………………………………………………. 3 1.2.2. Timing of initial inflation…………………………………………………… 5 1.3. Swimbladder non-inflation in teleosts………………………………………….. 7 1.3.1. Factors that were reported to affect SBN...…………………………………. 8 1.4. Angelfish Pterophyllum scalare………………………………………………... 12 1.4.1. Swimbladder non-inflation in Angelfish……………………………………. 13 1.5. Research objectives……………………………………………………………... 14 2. Materials and methods………………………………………………………… 15 2.1. Fish hatching and rearing protocol in “Negev Angels” commercial fish farm…. 15 2.2. Field survey of SBN prevalence………………………………………………… 15 2.3. Fish experimental system……………………………………………………….. 16 2.4. Effect of environmental factors on the prevalence of SBN in angelfish………... 16 2.4.1. Access to the air-water interface…………………………………………….. 17 2.4.2. Effect of methylene blue (disinfectant) concentration on SBN……………… 18 2.4.3. Effect of food concentration and starvation on SBN………………………… 18 2.4.4. Effect of water conductivity (salinity) on SBN……………………………… 19 2.4.5. Effect of tank coloration on SBN……………………………………………. 19 2.5. Histological characterization of normal and abnormal swimbladder development in early larval stages…………………………………………………………….. 19 2.5.1. Normal swimbladder development………………………………………….. 19 2.5.2. Abnormal swimbladder development……………………………………….. 21 2.6. Statistical analysis………………………………………………………………. 22 3. Results………………………………………………………………………….. 24 3.1. Survey of SBN prevalence in a commercial angelfish farm during 2003-2005… 24 3.2. The effect of environmental factors on SBN in anglefish……………………… 25 3.3. Histological characterization of normal and abnormal swimbladder development in early larval stages…………………………………………………………….. 26 3.3.1. Normal swimbladder development in anglefish…………………………….. 26 3.3.2. Abnormal swimbladder developmet under routine conditions……………… 40 3.3.3. Abnormal swimbladder development in larvae hatched in 5 ppm methyelene blue…………………………………………………………………………... 44 4. Discussion………………………………………………………………………. 55 5. Further research……………………………………………………………….. 71 6. Reference……………………………………………………………………….. 72 V List of tables Page Table 1. Number of eggs per replicate used in each experiment…………………… 17 Table 2. The effect of environmental factors on SBN/live fish……………………. 25 Table 3. Summary of characteristics of different abnormal swimbladder types appearing on the 4th day p.h……………………………………………… 47 List of figures Page Figure 1. A net box used to prevent the access to the air-water interface………… 18 Figure 2. Mean prevalence of SBN from live fish per month (%) in “Negev angels” commercial fish farm, during 2003-2005 ……………………………… 24 Figure 3. Larvae of angelfish Pterophyllum scalare at day 0 p.h…………………. 32 Figure 4. Larvae of angelfish Pterophyllum scalare at day 1 p.h…………………. 33 Figure 5. Larvae of angelfish Pterophyllum scalare at day 2 p.h…………………. 34 Figure 6. Larvae of angelfish Pterophyllum scalare at day 3 p.h…………………. 35 Figure
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