Effects of simulated microgravity on the development of the swimbladder and buoyancy control in larval zebrafish (Danio rerio).

The gas-filled swimbladder of teleost fishes provides hydrodynamic lift which counteracts the high density of other body tissues, and thereby allows the fish to achieve neutral buoyancy with minimal energy expenditure. In this study, we examined whether the absence of a constant direction gravitational vector affects the ontogeny of the swimbladder and buoyancy control in zebrafish (Danio rerio). We exposed fertilized eggs to simulated microgravity (SMG) in a closed rotating wall vessel with control eggs placed in a similar but nonrotating container. All eggs hatched in both groups. At 96 hr of postfertilization (hpf), all larvae were removed from the experimental and control vessels. At this point, 62% of the control larvae, but only 14% of SMG-exposed larvae, were observed to have inflated their swimbladder. In addition, the mean volume of the inflated swimbladders was significantly greater in the control larvae compared with larvae raised in SMG. After transfer to open stationary observation tanks, larvae with uninflated swimbladders in both groups swam to the surface to complete inflation, but this process was significantly delayed in larvae exposed to SMG. Initial differences in swimbladder inflation and volume between groups disappeared by 144 hpf. Furthermore, there were no apparent changes in patterns of development and maturation of swimbladder musculature, vasculature, or innervation resulting from SMG exposure at later stages of ontogeny. These data indicate that, despite a transient delay in swimbladder inflation in zebrafish larvae exposed to SMG, subsequent swimbladder development in these animals proceeded similarly to that in normal larvae.

[1]  M Yamashita,et al.  The mechanics of air-breathing in anuran larvae: implications to the development of amphibians in microgravity. , 2000, Advances in space research : the official journal of the Committee on Space Research.

[2]  B. Riley,et al.  Development of utricular otoliths, but not saccular otoliths, is necessary for vestibular function and survival in zebrafish. , 2000, Journal of neurobiology.

[3]  R. Croll,et al.  From inflation to flotation: contribution of the swimbladder to whole-body density and swimming depth during development of the zebrafish (Danio rerio). , 2010, Zebrafish.

[4]  M. Kiyomoto,et al.  Morphogenesis and gravity in a whole amphibian embryo and in isolated blastomeres of sea urchins. , 2003, Advances in space biology and medicine.

[5]  K. Rottner,et al.  Visualising the actin cytoskeleton , 1999, Microscopy research and technique.

[6]  B. Chatain,et al.  A sorting method for eliminating fish larvae without functional swimbladders , 1992 .

[7]  Wenyuan Gao,et al.  A critical period for gravitational effects on otolith formation. , 2003, Journal of vestibular research : equilibrium & orientation.

[8]  The behavioral reactions of a snake and a turtle to abrupt decreases in gravity. , 1993, Zoological science.

[9]  R. Anken,et al.  Effects of altered gravity on the swimming behaviour of fish. , 2002, Advances in space research : the official journal of the Committee on Space Research.

[10]  S. Battaglene,et al.  A finite interval of initial swimbladder inflation in Latris lineata revealed by sequential removal of water‐surface films , 2005 .

[11]  Eberhard R Horn,et al.  Microgravity-induced modifications of the vestibuloocular reflex in Xenopus laevis tadpoles are related to development and the occurrence of tail lordosis , 2006, Journal of Experimental Biology.

[12]  W. K. Metcalfe,et al.  Primary neurons that express the L2/HNK-1 carbohydrate during early development in the zebrafish. , 1990, Development.

[13]  C. Dournon Developmental biology of urodele amphibians in microgravity conditions. , 2003, Advances in space biology and medicine.

[14]  R. Summerfelt,et al.  Microvideography of gas bladder inflation in larval walleye , 1998 .

[15]  E. Denton The buoyancy of fish and cephalopods. , 1961, Progress in biophysics and molecular biology.

[16]  K. Ijiri Life-cycle experiments of medaka fish aboard the international space station. , 2003, Advances in space biology and medicine.

[17]  S. Nagaoka,et al.  Nitrate toxicity on visceral organs of Medaka fish, Oryzias latipes: aiming to raise fish from egg to egg in space. , 2004, Uchu Seibutsu Kagaku.

[18]  Enno Brinckmann New facilities and instruments for developmental biology research in space. , 2003, Advances in space biology and medicine.

[19]  D. Stainier,et al.  Isolation of the zebrafish homologues for the tie‐1 and tie‐2 endothelium‐specific receptor tyrosine kinases , 1998, Developmental dynamics : an official publication of the American Association of Anatomists.

[20]  F. Strollo Hormonal changes in humans during spaceflight. , 1999, Advances in space biology and medicine.

[21]  R. Croll,et al.  The contribution of the swimbladder to buoyancy in the adult zebrafish (Danio rerio): A morphometric analysis , 2008, Journal of morphology.

[22]  W. Chavin The Physiology of Fishes , 1957, The Yale Journal of Biology and Medicine.

[23]  E. Snetkova,et al.  Effects of space flight on Xenopus laevis larval development. , 1995, The Journal of experimental zoology.

[24]  H Rahmann,et al.  Gravitational neurobiology of fish. , 2000, Advances in space research : the official journal of the Committee on Space Research.

[25]  V R Edgerton,et al.  Human fiber size and enzymatic properties after 5 and 11 days of spaceflight. , 1995, Journal of applied physiology.

[26]  E. Goolish,et al.  Lack of gas bladder inflation by the larvae of zebrafish in the absence of an air‐water interface , 1999 .

[27]  Felice Strollo,et al.  Chapter 4 Hormonal Changes in Humans During Spaceflight , 1999 .

[28]  J. B. Steen,et al.  10 The Swim Bladder as a Hydrostatic Organ , 1970 .

[29]  C. Burress,et al.  Stimulus dependence of the development of the zebrafish (Danio rerio) vestibular system. , 1999, Journal of neurobiology.

[30]  R. Croll,et al.  Development of the swimbladder and its innervation in the zebrafish, Danio rerio , 2007, Journal of morphology.

[31]  N. Shimada,et al.  Changes in gravitational force affect gene expression in developing organ systems at different developmental times , 2005, BMC Developmental Biology.

[32]  Denton Ej The buoyancy of fish and cephalopods. , 1961 .

[33]  S. Moorman,et al.  A critical period for functional vestibular development in zebrafish , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[34]  S. Nilsson Nervous control of fish swimbladders. , 2009, Acta histochemica.

[35]  K. Walton,et al.  Long‐term effects of microgravity on the swimming behaviour of young rats , 2005, The Journal of physiology.

[36]  R. Wassersug,et al.  Amphibian development in the virtual absence of gravity. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[37]  E. Horn Xenopus laevis – a success story of biological research in space , 2004 .

[38]  H. Ohgushi,et al.  The Effect of Simulated Microgravity by Three-Dimensional Clinostat on Bone Tissue Engineering , 2005, Cell transplantation.

[39]  E. Horn,et al.  The minimum duration of microgravity experience during space flight which affects the development of the roll induced vestibulo-ocular reflex in an amphibian (Xenopus laevis) , 1998, Neuroscience Letters.

[40]  NationalResearchCouncil,et al.  A Strategy for Research in Space Biology and Medicine in the New Century , 1998 .

[41]  J. Sedat,et al.  Fluorescence microscopy: reduced photobleaching of rhodamine and fluorescein protein conjugates by n-propyl gallate. , 1982, Science.

[42]  J. Vernikos Human physiology in space. , 1996, BioEssays : news and reviews in molecular, cellular and developmental biology.

[43]  John M. Dettmers,et al.  Ecological Consequences of Swim Bladder Noninflation for Larval Yellow Perch , 2005 .

[44]  R. Anken,et al.  Readaptation of fish to 1g after long-term microgravity: behavioural results from the STS 89 mission. , 2000, Advances in space research : the official journal of the Committee on Space Research.

[45]  R. Croll,et al.  Structure and autonomic innervation of the swim bladder in the zebrafish (Danio rerio) , 2006, The Journal of comparative neurology.

[46]  D M Webber,et al.  Costs of Locomotion and Vertic Dynamics of Cephalopods and Fish* , 2000, Physiological and Biochemical Zoology.

[47]  Bruce R. Friedmann,et al.  Effect of Timing of Oil Film Removal and First Feeding on Swim Bladder Inflation Success among Intensively Cultured Striped Bass Larvae , 1999 .