The Legacy of Hypoxia: Tracking Carryover Effects of Low Oxygen Exposure in a Demersal Fish Using Geochemical Tracers

Abstract

The increasing prevalence of hypoxia in aquatic ecosystems emphasizes the need to understand sublethal effects on organisms to anticipate potential changes in population dynamics. Carryover effects of hypoxia exposure during early life stages on lifetime survival and growth performance are rarely known, which leaves major knowledge gaps about the long-term impacts of sublethal exposures. Geochemical signatures incorporated into fish hard parts can track lifetime hypoxia exposure, thereby allowing sublethal carryover effects across age-classes to be quantified. We examined the impact of hypoxia exposure on the Atlantic Croaker Micropogonias undulatus, a demersal fish inhabiting the northern Gulf of Mexico, which is one of the largest hypoxic systems in the world. Using an otolith-based, dual-proxy (Mn:Ca and Ba:Ca) geochemical method coupled with intracohort comparisons, we assessed changes in the traits of Atlantic Croakers that survived hypoxia exposure during their first year of life. We also investigated whether somatic growth was affected by exposure to sublethal hypoxia during the first year of life. Within three cohorts of Atlantic Croakers, there was no evidence that the otolith-based traits of survivors changed from one year to the next. Additionally, somatic growth in individuals that had previously experienced sublethal hypoxia during the first year of life and survived was not depressed relative to somatic growth in individuals that did not experience hypoxic conditions. These results indicate that Atlantic Croakers are tolerant to hypoxia experienced during early life and that sublethal carryover effects do not manifest as reductions in survival or growth. Geochemical indicators of hypoxia exposure in fish otoliths can thus provide vital insight into the range of potential sublethal responses by fishes with variable sensitivities to this growing environmental stressor across the world.

It’s elemental, my dear Watson: validating seasonal patterns in otolith chemical chronologies

“…Interest in the chemical composition, often termed "microchemistry", of otoliths has been increasing steadily over the last two decades (see reviews in Campana (1999) and Sturrock et al (2012)). The primary focus of these studies has been the reconstruction of environmental exposure, notably the use of strontium (Sr), barium (Ba) and manganese (Mn) to infer migrations between areas with different salinities (Kraus and Secor, 2004;Sturrock et al, 2012) or hypoxia exposure (Altenritter and Walther, 2019;Limburg et al, 2011;Mohan and Walther, 2016) and other elements as tracers of anthropogenic contamination (Ranaldi and Gagnon, 2008). Elements that are under physiological control, such as phosphorus (P) and zinc (Zn), on the other hand, have received far less attention (Campana, 1999).…”

Effects of spatial variability on the exposure of fish to hypoxia: a modeling analysis for the Gulf of Mexico

“…Most examples under field conditions use indirect measurements to show exposure of fish to hypoxia at some time in the past. These indirect methods include chemical tracers (Limburg et al, 2015;Altenritter and Walther, 2019), molecular indicators (Brouwer et al, 2005), and biomarkers (Thomas et al, 2007). Relatively few analyses report on the detailed recording of exposure of fish as they move within dynamic DO fields.…”

Otolith chemoscape analysis in whiting links fishing grounds to nursery areas

“…Each "point" sample, calculated as the midpoint of the trawl, therefore, actually represents an area of uncertainty (presumably < 78 km) around the trawl location. A suite of 17 elements ( 7 Li, 23 Na, 24 Mg, 27 Al, 31 P, 45 Sc, 47 Ti, 52 Cr, 55 Mn, 60 Ni, 65 Cu, 66 Zn, 85 Rb, 88 Sr, 89 Y, 138 Ba, 208 Pb) was selected to maximise the chance of observing spatial variability and sampled using LA-ICP-MS. Sr and Ba have been shown to vary with temperature and salinity 39,40 . Al, P, Cu and Pb may be present at higher concentrations where anthropogenic inputs raise their levels in the environment, and this may be reflected in the trace element concentrations found in otoliths from fish sampled in areas like the east Irish Sea and Firth of Clyde.…”

“…Temporally persistent regional otolith signatures of Ba and Mn have also been documented occurring in UK waters 41 . While Mn and Mg have been recognised as a biomineralization cofactors involved in otolith formation 50,51 , the concentration of Mn in otoliths has also been explained by extrinsic factors like hypoxia 52 . Although there are yet no definitive explanations for the mechanisms governing observed differences in otolith concentrations of many elements, the spatial variation reported in the current study has allowed the construction of cross-validated chemoscapes from sampled otolith material.…”

“…Element composition was analysed using a PerkinElmer Elan DRCII + ICP-MS (PerkinElmer, Buckinghamshire, UK) equipped with a New Wave Research UP213 laser ablation system (LA-ICP-MS), using helium gas (flow = 0.8 L min −1 ) as the carrier and argon plasma (flow = 0.75 L min −1 ). The presence of 18 element isotopes ( 7 Li, 23 Na, 24 Mg, 27 Al, 31 P, 44 Ca, 45 Sc, 47 Ti, 52 Cr, 55 Mn, 60 Ni, 65 Cu, 66 Zn, 85 Rb, 88 Sr, 89 Y, 138 Ba, 208 Pb) were analysed. Pre-ablation transects (100 µm wide) were run in order to decontaminate the surface before a series of 55 µm diameter pits were sampled for a dwell time of 20 s (~50 µm deep) from the core to the edge of each otolith (6 for age-0 and 12 for age-1).…”