Out of breath and hungry: the effects of hypoxia on feeding dynamics of Atlantic croaker using natural chemical tags

By John Mohan 
2015 Recipient of Estuaries Section Student Travel Award
University of Texas at Austin. Marine Science Institute.

Author John Mohan taking a water sample.

Hypoxia, or low dissolved oxygen, occurs in many aquatic ecosystems across the world. Hypoxia is a natural phenomenon that requires specific conditions to form. These factors include stratification between surface and bottom waters and increased primary production resulting in algal blooms due to increased nutrient inputs. Nutrients are delivered via river water, which transport agricultural fertilizers and urban wastewater from inland areas to distant coastal locations. When higher amounts of nutrients are put into an aquatic system, typically lower concentrations of dissolved oxygen occur in bottom waters. The Mississippi River drains one of the largest watersheds in the United States, which contributes to nutrient enrichment in the northern Gulf of Mexico coastal zone. The hypoxic zone in the northern Gulf is famously known as the ‘Dead Zone,’ referring to the high mortality of benthic organisms, especially for species with limited mobility.

Previous studies have demonstrated a wide diversity of effects of hypoxia exposure on Atlantic croaker, ranging from enhanced foraging to reproductive impairment. These studies have utilized short-term trophic and molecular markers such as stomach content analysis and expression of hypoxia-related genes, revealing exposure information on the scale of days. However, mobile fish may swim away and avoid hypoxia, aggregate near the edges of hypoxia to capitalize on stressed prey, or experience habitat compression to regions of suboptimal conditions resulting in reduced growth rates. Few studies to date have utilized long-term markers of hypoxia exposure, such as otolith (ear stone) chemistry, in combination with long-term markers of dietary history such as tissue stable isotopes, to link chronic sub-lethal hypoxia exposure to changes in food web dynamics.

Otoliths, calcified structures forming part of the inner ear organ, constantly accrete layers as fish grow and can be used to determine fish age, and reveal environmental exposure histories. As otoliths grow, dissolved elements from the environment pass through the gills, enter the blood, and get deposited into the calcified otolith layers, providing a permanent record of the environment a fish occupied. For example, the element barium is found in low concentration in marine habitats, but high concentration in freshwater habitats. When fish migrate across salinity gradients the barium concentration in the otolith layer reflects fish migration between habitats. The element manganese is redox sensitive, meaning it will display high dissolved concentration at low oxygen levels. It was hypothesized that fish exposed to hypoxic conditions would incorporate higher dissolved manganese into their otoliths, and thus otolith manganese could be used as a proxy of the oxygen conditions a fish experienced over its entire life.

This research utilized both controlled experiments and natural field collections to explore the effects of hypoxia on Atlantic croaker trophic ecology in the northern Gulf of Mexico using a dual natural chemical tag approach. Otolith chemistry was used to determine the level of hypoxia exposure fish experienced throughout life and muscle tissue stable isotopes were used to examine the long-term dietary history of the same fish. Laboratory experiments provided validation of otolith-water chemistry relationships and diet-tissue stable isotope relationships that were essential for accurate interpretation of data from natural croaker collections in the northern Gulf hypoxic zone.

In the northern Gulf of Mexico ‘Dead Zone’ Atlantic croakers and water samples were collected from locations with low oxygen and high oxygen concentrations during the fall and summer seasons. Trace element profiles in otoliths of croaker were used to estimate environmental exposure histories over the 2-3 months prior to capture. Otoliths were analyzed using a laser across the growth bands to quantify profiles of manganese as an indicator of oxygen conditions and barium as a proxy of salinity conditions and estuarine habitat use. It was important to differentiate between inshore estuarine and coastal habitat residence because the croaker are highly mobile. Estuarine residence and hypoxia exposure indices were developed based on otolith chemistry, and used to identify similar groups of fish that included late estuarine migrants, early estuarine migrants, coastal residents, and hypoxic coastal resident fish. Muscle tissue stable isotope values of carbon and nitrogen that also reflected 2-3 months of recent dietary history were then used to estimate isotope niche areas that describe the overall diversity of fish diet. Fish demonstrating more estuarine habitat use displayed larger niche areas, while normoxic and hypoxic coastal resident fish exhibited small and statistically similar niche areas. Similarity in trophic measures between hypoxic and normoxic fish suggest trophic resilience of demersal croaker to hypoxia in the northern Gulf of Mexico over seasonal time scales. A combination of otolith chemistry and tissue stable isotopes further enhances our understanding of fish responses to sublethal hypoxia and the potential consequences for ecosystem functioning.

John Mohan measuring a spotted seatrout (Cynoscion nebulosus) before implanting an acoustic tag for a movement study sponsored by the Nature Conservancy at Half Moon Reef in Matagorda Bay, TX.