Publications

Peer-Reviewed Publications

Fisheries Research

Limburg, K.E., Heimbrand, Y., Hüssy, K., Blass, M., Thomas, J.B., Mäkinen, K. Næraa, T.: The forgotten element: Why do we ignore calcium in otolith studies? Fisheries Research 283 (2025) 107297, https://doi.org/10.1016/j.fishres.2025.107297

Abstract: Typical analyses of otolith microchemistry use calcium, a major constituent, as an internal standard, setting its value as a constant and ignoring any potential variations. In fact, patterns do occur in otolith Ca deposition, as can be observed either by repeating the analysis, by creating two-dimensional maps of Ca, or both. Here we present evidence of Ca variations in fish otoliths from analyses using synchrotron-based scanning X-ray fluorescence microscopy, electron microprobe analysis, and laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS). 2-D maps of otoliths created with LA-ICP-MS indicate that Ca is elevated where especially Zn and P are low, and vice versa, suggesting that spatial variations in protein deposition may affect concentrations of Ca. We encourage others to examine Ca concentrations in their biomineralized samples to check for variations, using LA-ICP-MS and other methods.

canadian Journal of Fisheries and Aquatic Sciences

Miraly, H., Razavi, R., Kraus, R.T., Gorman, A.M., Duskey, E., Altenritter, M., Limburg, K.E.: Using complementary biomarkers to unravel fish lifetime exposure to hypoxia and mercury. Can. J. Fish. Aquat. Sci. 82: 1–12 (2025) | dx.doi.org/10.1139/cjfas-2024-0235. https://cdnsciencepub.com/eprint/ZPRFIPMJDJ9UAX7TXDHS/full

Abstract: Aquatic ecosystems are losing oxygen due to climate change. This deoxygenation can favor microbial methylation of mercury (Hg). To understand the dynamics of Hg under increasing deoxygenation, we simultaneously quantified both Hg and hypoxia (<2 mg O2·L−1) lifetime chronologies in fishes. We used a novel combination of chemical biomarkers in ear stones and eye lenses. We compared these markers in two species with different life histories, benthic round goby (Neogobius melanostomus) and semi-demersal yellow perch (Perca flavescens), from two connected ecosystems with different levels of hypoxia: the Central Basin of Lake Erie and the less hypoxic but more polluted Western Basin. Overall, Central Basin round goby were exposed to hypoxia throughout their lifetime and exhibited significantly elevated eye lens Hg concentrations ([Hg]) compared to their Western Basin counterparts. In contrast, the Central Basin yellow perch were exposed to hypoxia only at their juvenile stage. Central Basin yellow perch exhibited significantly lower eye lens [Hg] compared to their Western Basin counterparts. Patterns revealed by eye lens [Hg] were not detectable in muscle tissue [Hg]. Findings show that exposure to hypoxia can alter fish lifetime Hg accumulation patterns, with species-specific outcomes.

Frontiers In Ecology and the Environment

Limburg, K.E. (2024), Deoxygenation—coming to a water body near you. Front Ecol Environ, 22: e2812. https://doi.org/10.1002/fee.2812

Description: A guest editorial discussing the issue of deoxygenation in marine and inland waters, and highlighting the accomplishments of the UNESCO–Intergovernmental Oceanographic Commission working group, the Global Ocean Oxygen Network (GO2NE).

scientific Reports

Heimbrand, Y., Limburg, K. E., Hüssy, K., Næraa, T., Casini, M: Cod otoliths document accelerating climate impacts in the Baltic Sea. Scientific Reports, 2024, 14:16750, https://doi.org/10.1038/s41598-024-67471-2

Abstract: Anthropogenic deoxygenation of the Baltic Sea caused major declines in demersal and benthic habitat quality with consequent impacts on biodiversity and ecosystem services. Using Baltic cod otolith chemical proxies of hypoxia, salinity, and fish metabolic status and growth, we tracked changes from baseline conditions in the late Neolithic (4500 BP) and early twentieth century to the present, in order to understand how recent, accelerating climate change has affected this key species. Otolith hypoxia proxies (Mn:Mg) increased with expanding anoxic water volumes, but decreased with increasing salinity indexed by otolith Sr:Ca. Metabolic status proxied by otolith Mg:Ca and reconstructed growth were positively related to dissolved oxygen percent saturation, with particularly severe declines since 2010. This long-term record of otolith indicators provides further evidence of a profound state change in oxygen for the worse, in one of the world’s largest inland seas. Spreading hypoxia due to climate warming will likely impair fish populations globally and evidence can be tracked with otolith chemical biomarkers.

Biogeosciences

Limburg, K. E., Heimbrand, Y., and Kuliński, K.: Marked recent declines in boron in Baltic Sea cod otoliths – a bellwether of incipient acidification in a vast hypoxic system?, Biogeosciences, 20, 4751–4760, https://doi.org/10.5194/bg-20-4751-2023, 2023.

Abstract: Ocean acidification is spreading globally as a result of anthropogenic CO2 emissions, but the Baltic Sea has until recently been thought to be relatively well-buffered by terrigenous inputs of alkalinity from its watershed. We discovered a 3- to 5-fold decline in boron (as B : Ca) in otoliths of eastern Baltic cod (EBC) between the late 1990s and 2021. Examining a time series of EBC otoliths, we found varying levels of B : Ca starting in the 1980s, with the most recent years showing an all-time low for this period. This trend correlates with declines in pH and dissolved oxygen but not with changes in salinity. We examined possible physiological influences on B : Ca by including a collection of Icelandic cod as an “out-group”. Icelandic cod otoliths showed strongly positive correlations of B : Ca with physiologically regulated P : Ca; this was not the case for EBC. Finally, B : Ca in EBC otoliths is negatively correlated, to some extent, with Mn : Mg, a proposed proxy for hypoxia exposure. This negative relationship is hypothesized to reflect the dual phenomena of hypoxia and acidification as a result of decomposition of large algal blooms. Taken together, the otolith biomarkers Mn : Mg and B : Ca in cod suggest a general increase in both hypoxia and acidification within the Baltic intermediate and deep waters in the last decade.

Frontiers in Marine Science

Duskey E (2023) Metabolic prioritization of fish in hypoxic waters: an integrative modeling approach. Front. Mar. Sci. 10:1206506. doi: 10.3389/fmars.2023.1206506 https://www.frontiersin.org/articles/10.3389/fmars.2023.1206506/full

Abstract: Marine hypoxia has had major consequences for both economically and ecologically critical fish species around the world. As hypoxic regions continue to grow in severity and extent, we must deepen our understanding of mechanisms driving population and community responses to major stressors. It has been shown that food availability and habitat use are the most critical components of impacts on individual fish leading to observed outcomes at higher levels of organization. However, differences within and among species in partitioning available energy for metabolic demands – or metabolic prioritization – in response to stressors are often ignored. Here, I use both a multispecies size spectrum model and a meta-analysis to explore evidence in favor of metabolic prioritization in a community of commercially important fish species in the Baltic Sea. Modeling results suggest that metabolic prioritization is an important component of the individual response to hypoxia, that it interacts with other components to produce realistic community dynamics, and that different species may prioritize differently. It is thus suggested that declines in feeding activity, assimilation efficiency, and successful reproduction – in addition to low food availability and changing habitat use – are all important drivers of the community response to hypoxia. Meta-analysis results also provide evidence that the dominant predator in the study system prioritizes among metabolic demands, and that these priorities may change as oxygen declines. Going forward, experiments and models should explore how differences in priorities within and among communities drive responses to environmental degradation. This will help management efforts to tailor recovery programs to the physiological needs of species within a given system.

Environmental science & technology letters

Miraly, H. Razavi, R.N., Vogl, A.A., Kraus, R.T., Gorman, A.M., Limburg, K.E. (2022). Tracking Fish Lifetime Exposure to Hypoxia Using Eye Lenses. Environ. Sci. Technol. Lett. https://pubs.acs.org/doi/10.1021/acs.estlett.2c00755

Abstract: Mercury (Hg) uptake in fish is affected by diet, growth, and environmental factors such as primary productivity or oxygen regimes. Traditionally, fish Hg exposure is assessed using muscle tissue or whole fish, reflecting both loss and uptake processes that result in Hg bioaccumulation over entire lifetimes. Tracking changes in Hg exposure of an individual fish chronologically throughout its lifetime can provide novel insights into the processes that affect Hg bioaccumulation. Here we use eye lenses to determine Hg uptake at an annual scale for individual fish. We assess the widely distributed benthic round goby (Neogobius melanostomus) from the Baltic Sea, Lake Erie, and the St. Lawrence River. We aged layers of the eye lens using proportional relationships between otolith length at age and eye lens radius for each individual fish. Mercury concentrations were quantified using laser ablation inductively coupled plasma mass spectrometry. The eye lens Hg content revealed that Hg exposure increased with age in Lake Erie and the Baltic Sea but decreased with age in the St. Lawrence River, a trend not detected using muscle tissues. This novel methodology for measuring Hg concentration over time with eye lens chronology holds promise for quantifying how global change processes like increasing hypoxia affect the exposure of fish to Hg.

deep Sea Research

Cavole. L.M., Limburg, K.E., Gallo, N.D., Salvanes, A.G.V., Ramirez-Valdez, A., Lefin, L.A., Oropeza, O.A., Hertwig, A., Liu, M.C., McKeegan, K.D. (2023). Otoliths of marine fishes record evidence of low oxygen, temperature and pH conditions of deep Oxygen Minimum Zones. Deep Sea Research Part 1: Oceanographic Research Papers. Vol 191. https://doi.org/10.1016/j.dsr.2022.103941

Abstract: The deep-sea is rapidly losing oxygen, with profound implications for marine organisms. Within Eastern Boundary Upwelling Systems, such as the California and the Benguela Current Ecosystems, an important question is how the ongoing expansion, intensification and shoaling of Oxygen Minimum Zones (OMZs) will affect deep-sea fishes throughout their lifetimes. One of the first steps to filling this knowledge gap is through the development of tools and techniques to track fishes’ exposure to hypoxic (<45 μmol kg-1), low-temperature (∼4–10°C) and low-pH (∼7.5) waters when inhabiting OMZs. Here, we examine if the otoliths of deep-sea fishes living in OMZs exhibit distinct patterns of elemental and isotopic composition, which could be used to monitor their exposure history to severely hypoxic and low-pH waters. We hypothesize that the unique biogeochemistry of OMZs (i.e., low-oxygen, low-pH, and the presence of dissolved elements) will impart unique elemental and isotopic signatures upon the otoliths of both long-lived and short-lived deep-sea fishes living within it. We analyzed the otoliths of six deep-sea fish species from three OMZ regions: the Southern California Bight and the Gulf of California in the Northeast Pacific Ocean, and the Namibian shelf in the Southeast Atlantic Ocean. Three complementary techniques were applied: laser ablation inductively coupled plasma mass spectrometry, secondary ion mass spectrometry and scanning X-ray fluorescence microscopy. We observed that deep-water OMZ-dwelling fishes spanning a range of life-history traits (e.g., longevity, maximum size, growth rate, parental investment and thermal history inferred by δ18O) exhibited a common elemental fingerprint (with respect to Sr:Ca, Mn:Ca, Ba:Ca, Cu:Ca and Mg:Ca) when compared to a shallow-water marine fish from better-oxygenated waters. Our findings suggest that the underlying mechanism for the common elemental fingerprinting of otoliths of OMZ-dwelling fishes is attributed to the unique biogeochemistry found on the margins of these highly productive upwelling systems as well as the physiological constraints resident organisms are perennially exposed to, including low oxygen, pH and temperature conditions.

Bulletin of the Ecological Society of America

Steube, T.R., Altenritter, M.E., and B.D. Walther. 2021. Fish Ear Stones Track Hypoxia Exposure. Bulletin of the Ecological Society of America. https://esajournals.onlinelibrary.wiley.com/doi/10.1002/bes2.1889

A photo gallery that illustrates the article “Distributive stress: individually variable responses to hypoxia expand trophic niches in fish” by Tyler R. Steube, Matthew E. Altenritter, Benjamin D. Walther published in Ecology. https://doi.org/10.1002/ecy.3356.

Ambio

Orio, A., Y. Heimbrand, and K. Limburg. 2021. Deoxygenation impacts on Baltic Sea cod: Dramatic declines in ecosystem services of an iconic keystone predator. Early view: https://link.springer.com/article/10.1007/s13280-021-01572-4

Abstract: The intensified expansion of the Baltic Sea’s hypoxic zone has been proposed as one reason for the current poor status of cod (Gadus morhua) in the Baltic Sea, with repercussions throughout the food web and on ecosystem services. We examined the links between increased hypoxic areas and the decline in maximum length of Baltic cod, a demographic proxy for services generation. We analysed the effect of different predictors on maximum length of Baltic cod during 1978–2014 using a generalized additive model. The extent of minimally suitable areas for cod (oxygen concentration ≥ 1 ml l−1) is the most important predictor of decreased cod maximum length. We also show, with simulations, the potential for Baltic cod to increase its maximum length if hypoxic areal extent is reduced to levels comparable to the beginning of the 1990s. We discuss our findings in relation to ecosystem services affected by the decrease of cod maximum length.

Ecology

Steube, T.R., Altenritter, M.E., and B.D. Walther. 2021. Distributive Stress: individually variable responses to hypoxia expands trophic niches in fish. Ecology. https://esajournals.onlinelibrary.wiley.com/doi/epdf/10.1002/ecy.3356

Abstract: Environmental stress can reshape trophic interactions by excluding predators or rendering prey vulnerable depending on the relative sensitivity of species to the stressor. Classical models of food web responses to stress predict either complete predator exclusion from stressed areas or complete prey vulnerability if predators are stress tolerant. However, if the consumer response to the stress is individually variable, the result may be a Distributive Stress Model (DSM) whereby predators distribute consumption pressure across a range of prey guilds and their trophic niche is expanded. We test these models in one of the largest hypoxic “Dead Zones” in the world, the northern Gulf of Mexico, by combining geochemical tracers of hypoxia exposure and isotopic ratios to assess individual-level trophic responses. Hypoxia-exposed fish occupied niche widths that were 14.8% and 400% larger than their normoxic counterparts in two different years, consistent with variable displacement from benthic to pelagic food webs. The degree of isotopic displacement depended on the magnitude of hypoxia exposure. These results are consistent with the DSM model and highlight the need to account for individually variable sublethal effects when predicting community responses to environmental stress.

Biogeosciences

Casini, M., M. Hansson, A. Orio, A., and K. Limburg. 2021. Changes in population depth distribution and oxygen stratification are involved in the current low condition of the eastern Baltic Sea cod (Gadus morhua). Biogeosciences 18(4): 1321-1331.

Abstract: During the past 20 years, hypoxic areas have expanded rapidly in the Baltic Sea, which has become one of the largest marine “dead zones” in the world. At the same time, the most important commercial fish population of the region, the eastern Baltic cod, has experienced a drastic reduction in mean body condition, but the processes behind the relation between deoxygenation and condition remain elusive. Here we use extensive long-term monitoring data on cod biology and distribution as well as on hydrological variations to investigate the processes that relate deoxygenation and cod condition during the autumn season. Our results show that the depth distribution of cod has increased during the past 4 decades at the same time of the expansion, and shallowing, of waters with oxygen concentrations detrimental to cod performance. This has resulted in a progressively increasing spatial overlap between the cod population and low-oxygenated waters after the mid-1990s. This spatial overlap and the actual oxygen concentration experienced by cod therein statistically explained a large proportion of the changes in cod condition over the years. These results complement previous analyses on fish otolith microchemistry that also revealed that since the mid-1990s, cod individuals with low condition were exposed to low-oxygen waters during their life. This study helps to shed light on the processes that have led to a decline of the eastern Baltic cod body condition, which can aid the management of this population currently in distress. Further studies should focus on understanding why the cod population has moved to deeper waters in autumn and on analyzing the overlap with low-oxygen waters in other seasons to quantify the potential effects of the variations in physical properties on cod biology throughout the year.

One Earth

Limburg, K.E., D. Breitburg, D.P. Swaney, and G. Jacinto. 2020. Ocean deoxygenation: A primer. One Earth 2(1): https://doi.org/10.1016/j.oneear.2020.01.001

Abstract: Earth’s ocean is losing oxygen; since the mid-20th century, 1%–2% of the global ocean oxygen inventory has been lost, and over 700 coastal sites have reported new or worsening low-oxygen conditions. This “ocean deoxygenation” is increasing and of great concern because of the potential magnitude of adverse changes to both global and local marine ecosystems. Oxygen is fundamental for life and biogeochemical processes in the ocean. In coastal and shelf regions and semi-enclosed seas, over-fertilization of waters largely from agriculture, sewage, and airborne sources creates algal blooms that die and decay, consuming oxygen. Globally, climate warming both exacerbates the problems from eutrophication and reduces the introduction of oxygen to the interior of the ocean. We discuss mechanisms, scale, assessments, projections, and impacts, including impacts to human well-being, at the individual, community, and ecosystem levels. Deoxygenation together with other stressors presents a major environmental challenge to sustainability and human use of the ocean.

Journal of Fish Biology

Heimbrand, Y., K.E. Limburg, R. Hussy, M. Casini, R. Sjoberg, A. Palmen Bratt, S. Levinsky, A. Karpushevskaia, K Radtke, and J. Ohlund. 2020. Seeking the true time: Exploring otolith chemistry as an age-determination tool. Journal of Fish Biology 97(2): https://doi.org/10.1111/jfb.14422

Abstract: Fish otoliths' chronometric properties make them useful for age and growth rate estimation in fisheries management. For the Eastern Baltic Sea cod stock (Gadus morhua), unclear seasonal growth zones in otoliths have resulted in unreliable age and growth information. Here, a new age estimation method based on seasonal patterns in trace elemental otolith incorporation was tested for the first time and compared with the traditional method of visually counting growth zones, using otoliths from the Baltic and North seas. Various trace elemental ratios, linked to fish metabolic activity (higher in summer) or external environment (migration to colder, deeper habitats with higher salinity in winter), were tested for age estimation based on assessing their seasonal variations in concentration. Mg:Ca and P:Ca, both proxies for growth and metabolic activity, showed greatest seasonality and therefore have the best potential to be used as chemical clocks. Otolith image readability was significantly lower in the Baltic than in the North Sea. The chemical (novel) method had an overall greater precision and percentage agreement among readers (11.2%, 74.0%) than the visual (traditional) method (23.1%, 51.0%). Visual readers generally selected more highly contrasting zones as annuli whereas the chemical readers identified brighter regions within the first two annuli and darker zones thereafter. Visual estimates produced significantly higher, more variable ages than did the chemical ones. Based on the analyses in our study, we suggest that otolith microchemistry is a promising alternative ageing method for fish populations difficult to age, such as the Eastern Baltic cod.

Biology Letters

Limburg, K.E., and M. Casini. 2019. Otolith chemistry indicates recent worsened Baltic cod condition is linked to hypoxia exposure. Biology Letters 15(12): https://doi.org/10.1098/rsbl.2019.0352

Abstract: Deoxygenation worldwide is increasing in aquatic systems with implications for organisms' biology, communities and ecosystems. Eastern Baltic cod has experienced a strong decline in mean body condition (i.e. weight at a specific length) over the past 20 years with effects on the fishery relying on this resource. The decrease in cod condition has been tentatively linked in the literature to increased hypoxic areas potentially affecting habitat range, but also to benthic prey and/or cod physiology directly. To date, no studies have been performed to test these mechanisms. Using otolith trace element microchemistry and hypoxia-responding metrics based on manganese (Mn) and magnesium (Mg), we investigated the relationship between fish body condition at capture and exposure to hypoxia. Cod individuals collected after 2000 with low body condition had a higher level of Mn/Mg in the last year of life, indicating higher exposure to hypoxic waters than cod with high body condition. Moreover, lifetime exposure to hypoxia was even more strongly correlated to body condition, suggesting that condition may reflect long-term hypoxia status. These results were irrespective of fish age or sex. This implies that as Baltic cod visit poor-oxygen waters, perhaps searching for benthic food, they compromise their own performance. This study specifically sheds light on the mechanisms leading to the low condition of cod and generally points to the impact of deoxygenation on ecosystems and fisheries.

Dissertations and theses

Heimbrand, Yvette. (2021) Losing track of time: causes and solutions for the problematic determination of Baltic cod age. Doctoral dissertation, Swedish University of Agricultural Sciences, Ultuna, Sweden. https://pub.epsilon.slu.se/23429/1/heimbrand_y_210506.pdf

Miraly, Hadis. (2024) Microchemical Analysis of Fish Earstones and Eye Lenses to Assess Climate-Driven Deoxygenation on Aquatic Contamination.Doctoral dissertation, State University of New York, College of Environmental Science and Forestry, Syracuse, New York.

Samson, Melvin A. (2021) Otolith Microchemistry in Stressful Environments: Otoliths as Tools for Species Identification and as Recorders of Hypoxia Exposure. Doctoral dissertation, State University of New York, College of Environmental Science and Forestry, Syracuse, New York.

Valenza, Apria N. (2021) Manganese, Magnesium, and Micropogonias undulatus: Identifying Growth and Hypoxia Exposure Histories of Fish in the Northern Gulf of Mexico Using Otolith Microchemistry. Master’s thesis, Texas A&M – Corpus Christi.