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ABSTRACT Title of Dissertation: HARMFUL ALGAL BLOOM STRESSORS ALTER BEHAVIOR AND BRAIN ACTIVITY IN THE KILLIFISH, FUNDULUS HETEROCLITUS. James D. Salierno, Doctor of Philosophy, 2005 Dissertation Directed By: Associate Professor A. S. Kane Marine-Estuarine-Environmental-Science Harmful algal bloom (HAB) events are increasing in severity and frequency worldwide, and are known to severely impact fish populations. Impacts of HABs on fish, as well as other organisms, occur through toxic and physical stress. Behavioral and central nervous system (CNS) alterations can have direct consequences to the fitness and survival of individuals and populations. This study investigated and characterized alterations in social and swimming behaviors and brain activity in mummichog (Fundulus heteroclitus) exposed to HAB stressors. The mummichog is an ecologically important estuarine fish species exposed to a variety of HAB events in the wild. A behavioral analysis system was developed to study swimming and social behavior of fish and an immunohistochemistry technique was used to investigate alterations in neuronal activity as evidenced by c-Fos protein expression. HAB stressors included excitatory (domoic acid, brevetoxin) and inhibitory (saxitoxin) neurotoxic agents as well as direct exposures to the dinoflagellate Pfiesteria shumwayae and the diatom Chaetoceros concavicornis. P. shumwayae and C. concavicornis are HAB species that are known to induce mortality through physical trauma to fish. Brevetoxin exposure increased swimming and social behaviors whereas saxitoxin decreased these behaviors. The effects of saxitoxin on swimming and social behaviors were consistent with exposure to a fish anesthetic, MS-222. Similarly, it was found, through c-Fos expression, that the excitatory HAB neurotoxins brevetoxin and domoic acid, increased neuronal activity while saxitoxin decreased activity. Exposure to P. shumwayae and C. concavicornis, resulted in significant dose related increases in neuronal activity. Stressor-specific neuronal activity was greatest in the optic lobe, but was also found in the telencephalon with physical stressors increasing activity greater than chemical stressors. Results demonstrate that sublethal exposures to HAB neurotoxins can alter swimming and social behavior in mummichog and exposures to both neurotoxins and algae can alter neuronal activity. Alterations in brain activity, and knowledge of specific regions within the brain activated during stress, can provide insights into the control of fish behavior. Ultimately, HAB exposure related changes in neuronal signaling may alter behaviors, resulting in individual and population level alterations during HAB events. HARMFUL ALGAL BLOOM STRESSORS ALTER BEHAVIOR AND BRAIN ACTIVITY IN THE KILLIFISH, FUNDULUS HETEROCLITUS. By James D. Salierno Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park, in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2005 Advisory Committee: Associate Professor Andrew Kane, Chair Associate Professor Mary Christman Associate Professor Judd Nelson Associate Research Scientist Dan Fisher Dr. Jan Landsberg © Copyright by James D. Salierno 2005 Preface Harmful algal blooms (HAB) in the Middle Atlantic States and associated fish morbidity and mortality have increased in frequency and severity over the past several decades. The ability to predict and characterize environmental effects of different HAB species are essential to HAB remediation and control. This study was designed to investigate the effects of low level (sublethal) HAB stressor exposure on fish swimming behavior and brain activity. The goal was to investigate and quantify possible alterations in mummichog (Fundulus heteroclitus) swimming behavior and neuronal activity resulting from HAB exposure, demonstrating that fish can be affected by low level HAB stress, which may then alter individual and population dynamics in the environment. In order to accomplish this goal, a software program was developed for the analysis of schooling, shoaling, and individual behaviors in fish. The software system was then coupled to an existing videography system which allowed the capture of thirty minute video segments of schools and shoals of mummichog before, during, and after exposure to toxins. Additionally, predator avoidance and startle response behaviors were analyzed by designing a model predator (bird) and an auditory/vibratory stimulus. Predator avoidance and startle responses in mummichog were then tested before, during and after exposures. An acclimation study was conducted in addition to an exposure to tricaine methanesulfonate (MS-222), a common fish anesthetic, in order to validate the behavioral quantification system. The acclimation study consisted of measuring ii mummichog behavior over a 3 day period to obtain baseline activities and changes in behaviors over time. Exposure of fish to MS-222 was then conducted as a second validation and for comparison to HAB neurotoxins. Once the system was validated and data from the acclimation and MS-222 experiments analyzed, mummichog were then exposed to known HAB neurotoxins, brevetoxin (PbTx-2) and saxitoxin (STX). Behaviors are initiated and regulated though the CNS and neuronal signaling is essential for the proper responses to different stimuli. As such, investigations into possible alterations in brain activity resulting from HAB sublethal stressor exposure in fish were conducted. c-fos, an immediate early gene and its protein product, c-Fos, are indicators of neuronal activity and stress in mammals. The procedure used to quantify c-Fos protein in mammals was acquired and adapted for use in mummichog brains. A transport stress experiment was then conducted with mummichog to test the ability to quantify changes in c-Fos protein expression in stressed fish. Once changes in c-Fos expression were quantified in different regions of mummichog brains, mummichogs were exposed to HAB neurotoxins PbTx-2, STX, domoic acid DA, and HAB species, Pfiesteria shumwayae and Chaetoceros concavicornis. In addition, different regions of the brain were investigated in an attempt to discern if stress-specific regional expression in c-Fos occurred. iii Hypotheses: Ha (1). The software system designed for the quantification of schooling and shoaling behaviors will accurately describe alterations in mummichog behavior over an acclimation period and exposure to a fish anesthetic, MS- 222. A video-based analysis system will be developed to quantify swimming behaviors, including schooling and shoaling, in groups of mummichog. Computer digitizing hardware will be coupled with a specific software program developed for the analysis of fish movement. Thirty minute video segments will be complied, digitized, transformed into x,y coordinate data, and converted into behavioral endpoints. In addition, predator avoidance and startle response behaviors will be measured through the development of a predator model and an auditory/vibratory system. Analysis of the acclimation and MS-222 behavioral data will be used to validate the behavior quantification system. Ha (2). Exposure to sublethal concentrations of brevetoxin (PbTx-2) and saxitoxin (STX) will alter behaviors in groups of mummichog, Fundulus heteroclitus. The behavior quantification system will then be used to examine alterations in schooling and shoaling behaviors through time resulting from HAB neurotoxin exposure. The excitatory neurotoxin, PbTx-2 will increase schooling and shoaling behaviors and the paralytic neurotoxin, STX will decrease these iv swimming behaviors. Exposure to these neurotoxins will also alter both startle response and predator avoidance behaviors. Ha (3). Alterations in neuronal activity resulting from transport stress in mummichog will be quantified through c-Fos protein expression, measured by immunocytochemistry. Immunocytochemisty, an antibody labeling technique used in mammalian research to stain and quantify c-Fos expression, will be adapted for use in mummichog. A transport stress experiment will then be conducted to examine c-Fos expression in mummichog resulting from moderate stress exposure. Transport stressed mummichog will display increase c-Fos expression compared to control fish. This will provide a method to quantify alterations in CNS neuronal activity in the fish brain. Ha (4). Exposure to sublethal concentrations of PbTx-2, domoic acid (DA), STX, and a range of densities of the dinoflagellate P. shumwayae and the diatom C. concavicornis, will alter CNS neuronal activity, evidenced by altered c-Fos protein expression. Mummichog will be exposed to HAB stress, including neurotoxins and HAB species in order to examine alteration in neuronal activity. Excitatory (PbTx-2 and DA) and physical stressors (transport stress, P. shumwayae, and C. concavicornis) will increase neuronal signaling and c-Fos expression, while paralytic neurotoxins (STX) should block neuronal signaling and decrease c-Fos signaling when compared to control fish. v Ha (5). Different types of HAB stress (toxins vs. physical stress) will induce region specific alterations neuronal signaling, i.e., different stressors will increase activity in different locations within the brain. The immunocytochemisty technique provides information regarding alterations in brain activity to the level of individual neurons. Therefore, different stressor types will induce c-Fos proteins in different regions of the mummichog brain. Conclusions Exposure to
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