FRAM – High North Research Center for Climate and Environment

Digital edition 2024

The sins of the fathers: multigenerational impact of crude oil on fish

Spawned in millions, tiny cod and polar cod embryos are swept by currents into the unknown, helpless to threats along the way. Will they meet a predator? Will they be carried to places that are too hot or too cold? Will their journey end in a sheen of black gold?


By: Jasmine Nahrgang // UiT The Arctic University of Norway

Foto av torskeyngel i isvann
The polar cod, a keystone species in the Arctic, spends much of its time in and under sea ice. Photo: Jasmine Nahrgang / UiT The Arctic University of Norway.

Of the millions of cod eggs spawned, only a few will hatch. Even fewer will survive to eat their first prey. Crude oil is just one of the dangers they face. They will not recover from an exposure to these toxic chemicals dissolved in the water, even at infinitely low concentrations.

The question arises: does the health of the entire population hang in the balance? Probably not, because life for these embryonic fish is harsh and unforgiving, regardless of toxic chemicals. The spawning stock is resilient. Oblivious to the fate of their offspring, the parents may release millions of eggs again next year. So, is the spawning stock safe? Maybe not, after all.

Toxic compounds impact reproduction

Thousands of compounds, to a large part uncharacterized, come into play when crude oil and other petroleum products are spilled at sea. These compounds, too many to fully comprehend, have the potential to affect all life stages of fish. Commercially and ecologically important species, such as Atlantic cod and polar cod, are at risk. Whether these chemicals act individually, additively, or synergistically in these complex mixtures, they have the potential to disrupt critical processes during the reproductive phases of these fish.

For example, millions of eggs of the arctic keystone species polar cod are released prematurely in the dead of the polar night. Our recently published study shows that exposure to crude oil leads to an early onset of spawning. Surprising! Most other such studies find a delay in gamete production. Maybe the early spawning we saw was related to the timing of the exposure, late during gonad maturation.

Forsker som jobber med prøver av torsk
Leah Strople conducting histological analyses of polar cod gonads. Photo: Ireen Vieweg / UiT The Arctic University of Norway.
Foto av forskere som sjekker kjønnet på torsk
Ireen Vieweg, Velmurugu Puvanendran, and Øyvind Hansen sexing polar cod using ultrasound. Photo: Jasmine Nahrgang / UiT The Arctic University of Norway.

From one model species to another

What is the impact of parental exposure on next-generation offspring? And which parent mediates the effect? We cannot tell. Maternal and paternal effects can only be investigated through cross fertilization between gametes of control and exposed fish. But gametes from unexposed polar cod are still unripe when eggs from exposed parents are spawned. We need to change our model species to another gadid, the Atlantic cod. This batch spawner releases gametes every few days over several weeks, allowing fertilization of gametes across treatments. A new experiment can be conducted. Embryos are raised, and maternal and paternal effects can be disentangled.

Hard times for the offspring

Exposure of the mother weighs hardest on the early life stages; eggs are significantly smaller and accumulate some oil compounds. Two days following fertilization, maternally exposed embryos show an inhibition of embryogenesis pathways, visible through a transcriptome analysis. Four days after being fertilized, all maternally exposed embryos have perished. But paternal effects can also be seen: fewer larvae hatch, and they are shorter.

Figur
Illustration: Leah Strople / University of Bergen and UiT The Arctic University of Norway.

The sins of the fathers

How offspring develop and thrive is tightly connected to the parents’ life history. Through endocrine disruption, the first-generation offspring may be at risk. Toxic compounds can alter a parent’s crucial regulatory mechanisms, which in turn affect the quality of eggs and sperm. Growing oocytes accumulate toxic substances that may or may not impact the future developing embryo. Some compounds may cause “epigenetic” alterations to the DNA. Such alterations leave the DNA sequence unchanged, but affect how genes are permanently turned on or off. If these epigenetic changes are in reproductive cells, they can be passed from parents to offspring and through generations. The Sins of the Fathers may cast a shadow on their children and their children’s children.

Foto av forskere som jobber med torsk
Claudia Erhart and Paul Dubourg about to strip roe an Atlantic cod. Photo: Jasmine Nahrgang / UiT The Arctic University of Norway.

Is fish population health at stake?

The most sensitive life stage is not always the stage that exposes population vulnerability. Seemingly robust life stages may carry hidden flaws that could cause more harm than first assumed. ToxiGen, a new project funded by the Research Council of Norway, seeks to identify the mechanisms at play when crude oil changes the fishes’ spawning time window. Ultimately, the project aims to determine if effects can be passed down to generations that were never directly exposed. A comprehensive approach, encompassing not only sensitive early life stages of fish, but also seemingly resilient ones, is crucial as we work to safeguard our marine resources and in particular fish populations that contribute to fundamental ecosystem services.

Further reading

Strople LC, Vieweg I, Yadetie F, Odei DK, Thorsen A, Karlsen OA, Goksøyr A, Sørensen L, Sarno A, Hansen BH, Frantzen M, Hansen ØJ, Puvanendran V, Nahrgang J (2023) Spawning time in adult polar cod (Boreogadus saida) altered by crude oil exposure, independent of food availability. J Toxicol Environ Health Part A: 1–24, https://doi.org/10.1080/15287394.2023.2228535

The projects and the people

This work started in 2019 through the Nansen Legacy project with post-doctoral fellowship Ireen Vieweg (UiT The Arctic University of Norway) and master student Leah Strople (University of Bergen/UiT The Arctic University of Norway) as drivers of the first experiment on polar cod that also led to the first publication by Strople et al. (2023). In 2020, Claudia Erhart followed-up with the series of experiments on Atlantic cod (PARENTOX I and II projects) funded by the Fram Centre flagship MIKON and ARCEx. Since 2023, the work continues with the ToxiGen project funded by the Research Council of Norway. Throughout the years, this series of studies have been conducted in close collaboration with among others Anders Goksøyr, Odd André Karlsen and Fekadu Yadetie (University of Bergen), Lisbet Sørensen and Mari Creese (SINTEF Ocean), Marianne Frantzen (Akvaplan-niva) and Velmurugu Puvanendran and Øyvind Hansen (Nofima).


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