Award: OCE-1433759

Aquatic hypoxia, or water containing such low oxygen so as to be harmful to many higher forms of life, is expanding in the world's oceans, estuaries, and great lakes. Hypoxia can have many different kinds of effects on organisms, including physiological stress, slower growth, damaged reproduction, and even death. But some organisms can swim away from hypoxic waters, allowing them to survive even if they experienced hypoxia for a little while. We often do not know the full impacts of hypoxia because it is difficult to find out if a fish swam through hypoxic waters at some point earlier in its life. In order to answer questions about the full effects of hypoxia, we need an internal indicator of hypoxia exposure histories within organisms like fish. In a novel study, we developed and refined proxies of individual fish exposure to hypoxia by taking advantage of the "data-logging" properties of fish otoliths. Otoliths, which literally means "ear-stones," are small, calcium carbonate organs that form part of the fish's hearing and balance system. Otoliths grow throughout a fish's life, laying down growth rings much like trees do, and thus they provide a natural calendar-clock for every fish (Figure 1). Besides visual patterns, chemical information is incorporated as trace concentrations of various elements and isotopes. Lifetime records can be measured by taking fine-scale transects from the otolith core, which formed at birth, and continuing through the growth bands to the outer edge, which formed just before the fish was captured. Otolith elements can also be quantified by making two-dimensional maps of entire cross-sections of the structure (Figure 1c). In the case of hypoxia, we found that the trace element manganese (Mn), which is dissolved in the water at low oxygen levels, is available and is taken up by fish and eventually incorporated into the otoliths at the time of exposure. We found that Mn uptake is affected by the fish's growth rate as well as by low oxygen in surrounding waters. We discovered that another trace element, magnesium (Mg) is also sensitive to growth rate and appears to be related to metabolic rate in many fish taxa; but it is only indirectly sensitive to hypoxia. Thus, we can divide Mn by Mg concentrations to at least partly remove the influence of growth rate on the hypoxia proxy. We studied exposure and impacts in four fish species in three regions of the world known for chronic to severe hypoxia: the Baltic Sea (cod and flounder), the Gulf of Mexico (Atlantic croaker), and Lake Erie (yellow perch). In all species, the Mn/Mg proxy picks up the hypoxia signal. We find, however, that the responses to exposure are varied. Baltic Sea cod appear to be the most severely impacted by hypoxia; cod are in declining body condition (Figure 2). Heavily exposed cod have lost on average 39% of their length and 64% of their body weight at Age 3 compared to healthy cod (Figure 3). Their growth is further compromised by parasites and diseases that cannot be fought off due to lower metabolism caused by lack of oxygen. In the Gulf of Mexico, hypoxic waters form every summer because of warming surface waters and the massive inputs of nutrients and fertilizers from the Mississippi River that fuel massive blooms of phytoplankton which consume oxygen when they decompose. This creates a large area of hypoxia called the "Dead Zone." This "Zone" is patchy and changes in size over time, however, so the magnitude of fish exposure was unknown. Using our otolith tracking procedure, we found that between one-quarter to one-half of all Atlantic croaker showed evidence of hypoxia exposure in their first year of life. This means a large proportion of this fish survives hypoxia. There were no major apparent effects of the hypoxia exposure on growth of survivors, perhaps because Atlantic croaker have a greater physiological tolerance of low oxygen compared to a species like cod. However, croaker that experienced the most hypoxia showed evidence of significantly altering their food web interactions, perhaps as a result of swimming away from hypoxic waters at the bottom of the sea floor. These results highlight the complex responses of various fishes to hypoxic stress, and the responses can differ significantly depending on the species and system. Our project showed that internal chemical indicators within a fish can reveal an amazing amount of information about their movements and life history, including exposure to stressful hypoxic waters. Additionally, it led to a surprising discovery of a tracer of lifetime fish condition. Our results provided essential information about the magnitude of hypoxia exposure and the impacts on growth and performance of mobile fish species. Last Modified: 12/02/2019 Submitted by: Karin E Limburg