Recovery of Larval Sea Lampreys from Short‐Term Exposure to the Pesticide 3‐Trifluoromethyl‐4‐Nitrophenol: Implications for Sea Lamprey Control in the Great Lakes

Abstract

For over 50 years, invasive sea lamprey Petromyzon marinus populations have been controlled in the Great Lakes using the pesticide 3-trifluoromethyl-4-nitrophenol (TFM), which is applied to streams containing larval sea lampreys. The specificity of TFM is due to the sea lamprey's relative inability to detoxify it using glucuronidation; this inability causes death by interfering with the production of ATP, the main energy currency of cells. TFM treatments typically last 12 h, but given the sea lamprey's relative inability to detoxify TFM we predicted that TFM-induced homeostatic disturbances and toxicity would occur following shorter periods of exposure. Accordingly, we exposed larval sea lampreys to the 12-h LC99.9 (i.e., the concentration lethal to 99.9% of the test subjects over 12 h) of TFM for 4 or 6 h and monitored the survival and replenishment of energy stores and metabolite concentrations in surviving sea lampreys over a 24-h depuration period. Minimal mortality (∼20%) was observed during the post-TFM recovery, despite respective 50% and 70% reductions in brain and liver ATP, 70-90% decreases in brain phosphocreatine (PCr), and 30-50% reductions in brain and liver glycogen with corresponding increases in lactate. While relatively resistant to TFM, muscle still underwent a 55% decline in PCr. However, energy stores and metabolites returned to preexposure levels 4-12 h after TFM exposure. We conclude that sea lampreys can rapidly restore homeostasis following shorter-term TFM exposure. The resilience of sea lampreys to shorter-term TFM exposure suggests that there is no merit in reducing TFM treatment times from 12 h, which could lead to "treatment residuals" that survive lampricide treatments. This capacity to reverse TFM-induced perturbations also suggests that larvae seen emerging from the stream substrate late in a treatment, or that find refuge near streambanks or in isolated pools, could be another source of treatment residuals, leading to increased sea lamprey parasitism of sport and commercial fisheries in the Great Lakes.

The lampricide 3-trifluoromethyl-4-nitrophenol causes temporary metabolic disturbances in juvenile lake sturgeon (Acipenser fulvescens): implications for sea lamprey control and fish conservation

“…In recent years, a number of studies have described the physiological impact and mechanism of TFM toxicity in sea lamprey, non-target fishes and other organisms ( Viant et al , 2001 ; Wilkie et al , 2007 ; Birceanu et al , 2009 , 2011 , 2014 ; Clifford et al , 2012 ; Henry et al , 2015 ). Because of the structural similarity of TFM to 2,4-dinitrophenol (2,4-DNP), a known uncoupler of oxidative phosphorylation, it was first suggested by Applegate et al (1966 ) that TFM may cause death by interfering with mitochondrial ATP production.…”

“… Birceanu et al (2009 , 2011) later showed that TFM uncouples oxidative phosphorylation in mitochondria isolated from the livers of sea lamprey and in non-target rainbow trout, leading to a mismatch between ATP supply and ATP demand ( Birceanu et al , 2009 , 2014 ). Notably, TFM significantly depleted anaerobic energy stores such as glycogen and phosphocreatine in metabolically active tissues such as the brain, liver and kidney, but less so in the muscle ( Wilkie et al , 2007 ; Birceanu et al , 2009 , 2014 ; Clifford et al , 2012 ).…”

Post-exposure effects of the piscicide 3-trifluoromethyl-4-nitrophenol (TFM) on the stress response and liver metabolic capacity in rainbow trout (Oncorhynchus mykiss)

“…The TFM-induced increase in cortisol in vivo in the present context could be advantageous to the fish short-term immediately after TFM exposure, as it allows them to cope with and recover from the exposure. Short-term elevations of cortisol would be advantageous because cortisol promotes glycogenolysis [ 36 – 39 ], making more glucose available for metabolic processes [ 36 , 37 ], as the fish rely on glycolysis to meet the demands of the body during and following TFM exposure [ 5 – 7 , 12 ]. In addition, glycogenolysis provides glucose-6-phosphate, which is then used as a substrate for glucuronic acid production, a major player involved in pesticide detoxification via glucuronidation [ 40 ].…”

“…As previously stated, chronically elevated cortisol in fish can negatively impact the endocrine response to stressors long-term, leading to effects on gamete quality, survivability, progeny performance and may impact the overall social status and parental care ability of the adults. In addition, TFM leads to an increased reliance on anaerobic glycolysis to make up for shortfalls in ATP supply [ 6 , 7 , 12 ], and, if applied in the presence of additional exogenous stressors (e.g. adverse environmental conditions or food deprivation), it is possible that a fishes’ability to handle such stressors could be compromised.…”

Analysis of sea lamprey environmental DNA during lampricide treatment in a tributary of Lake Ontario

“…All sample sites fell within the range of the tributary that was treated. Exposure to TFM usually occurs over 12 hours for maximum lethality (Clifford et al, 2012) and TFM concentrations for 2017 treatments were designed to eliminate 93% of the larvae in the population (Sullivan and Mullett, 2018).…”