Clupeid Response to Stressors: The Influence of Environmental Factors on Thiaminase Expression

Abstract

Over the past five decades, a reproductive failure related to thiamine deficiency, referred to as thiamine deficiency complex (TDC), has been observed in valuable salmonine fishes in the Great Lakes and Finger Lakes in North America and the Baltic Sea in Europe. The cause of TDC has been linked to the consumption of clupeid fish, which contain high levels of a thiamine-destroying enzyme called thiaminase I (hereafter referred to as “thiaminase”). High activities of thiaminase have been reported from clupeids such as Alewife Alosa pseudoharengus, Gizzard Shad Dorosoma cepedianum and Atlantic (Baltic) Herring Clupea harengus, but no consistent explanation has accounted for the wide range of observed variation in levels of thiaminase in clupeids. Chronic stress can suppress the immune systems of Alewife and other fishes, thereby reducing the number of circulating white blood cells available to suppress bacteria. Because the presence of thiaminase has been associated with thiaminolytic bacteria isolated from Alewife viscera, we hypothesized that stressful conditions, which can potentially limit clupeid immune response or alter internal physiological conditions, could allow for thiaminase to be produced more efficiently by bacteria or thiaminolytic bacteria could proliferate, or both events could occur, resulting in a subsequent increase in thiaminolytic activity. In this study, Alewives and Gizzard Shad were exposed to severe winter temperatures and low food availability, respectively, in replicated pond experiments to evaluate the influence of stressful conditions on clupeid thiaminase activity. Though responses in circulating white blood cell counts and metrics of fish condition indicated that experimental treatments affected these clupeids, these effects were not related to increased thiaminase activity. The only significant treatment effect on clupeid thiaminase was an increase in mean thiaminase activity in Gizzard Shad from ponds where only high quality energy sources were available. These data indicate that variability in clupeid thiaminase may be related to diet composition.

Received June 19, 2012; accepted January 15, 2013

ACKNOWLEDGMENTS

We thank Tom Brooking, Lars Rudstam, Robert Johnson, Paul Bowser, Richard DeFrancisco, Joanne Messick, Steve Lamb, and William Ridge for valuable insights and equipment at the onset of this project. We thank Lisa Brown for conducting thiaminase analyses and Jennifer Sun for conducting white blood cell differential counts. Jennifer Sun, Lauren Gallaspy, Jillian Cohen, Geoffrey Steinhart, Dana Warren, Jason Robinson, Daniel Josephson, Peter Stevens, Beth Boisvert, Hannah Shayler, and the Cornell Pond Facility staff provided technical and logistic support. Madeleine Mineau, Alexandra Denby, Summer Rayne Oakes, Nathan Smith, Tara Bushnoe, Thomas Bell, Mark Dettling, Jeremiah Dietrich, Geofrey Eckerlin, Michael Estrich, Taylor McLean, Ned Place, Kirk Smith, and Theodore Treska provided support in the field. Richard DeFrancisco and Joanne Messick provided laboratory materials and training. New York Sea Grant provided funding for the Alewife tank and pond experiments under project number R/FBF-15. We are grateful to the staff of the Ecology Research Center at Miami University for support during the pond experiment. Gizzard Shad pond experiments were supported by a National Research Initiative (NRI) grant (OHOR-2003-01756) from the U.S. Department of Agriculture, and a Summer Workshop grant (Department of Zoology, Miami University).