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EDITORIAL article

Front. Mar. Sci., 22 September 2023
Sec. Global Change and the Future Ocean
This article is part of the Research Topic Immunity and Disease of Aquatic Organisms Under the Combined Impact of Anthropogenic Stressors: Mechanisms and Disease Outcomes View all 7 articles

Editorial: Immunity and disease of aquatic organisms under the combined impact of anthropogenic stressors: mechanisms and disease outcomes

Anett Kristin Larsen*Anett Kristin Larsen1*Elisabeth HolenElisabeth Holen2Helmut SegnerHelmut Segner3
  • 1Department of Medical Biology, UiT The Arctic University of Norway, Tromsø, Norway
  • 2Institute of Marine Research, Bergen, Norway
  • 3Institute for Fish and Wildlife Health, Vetsuisse Faculty, University of Bern, Bern, Switzerland

Anthropogenic activities have high impact on the world’s ecosystems and are strong drivers of environmental change. Modifications of habitats to fit the needs of society are causing severe effects including global warming, environmental degradation, biodiversity loss and mass extinction (Ceballos et al., 2015; Ceballos et al., 2017; USGCRP, 2017). Temperature changes are evident (IPCC, 2014) and climate change is fueling extreme weather events worldwide. The impact of warming, acidification and deoxygenation are already having a dramatic effect on the flora and fauna of the oceans with significant changes in distribution of populations and decline in sensitive species (Bijma et al., 2013). These climate-related alterations of aquatic species’ ecological conditions often occur in combination with the presence of other anthropogenic stressors, such as pollution (Groh et al., 2022), eutrophication (Chislock et al., 2013), or overfishing (Jackson et al., 2001). The cumulative impact of these multiple man-made stressors can have severe and often unexpected consequences on aquatic organisms (Crain et al., 2008; Shears and Ross, 2010; Segner et al., 2014).

There is strong evidence that the incidence and severity of diseases in both freshwater and marine environments are increasing, and this increase appears to be related at least in part to the cumulative impacts of multiple anthropogenic stressors (Johnson and Paull, 2011; Burge et al., 2014; Miller et al., 2014; Adlard et al., 2015; Rohr and Cohen, 2020; Byers, 2021; Hutson et al., 2023). The relationship between environmental stress and disease of aquatic organisms can involve diverse mechanisms and processes, but a major driver appears to be the impact of the stressors on immunity (Jacobson et al., 2003; Martin et al., 2010; Rollins-Smith, 2017; Palmer, 2018). Immunity is a convergence point for many environmental stressors, hence, changes in immune performance can be at the root of emerging disease. For instance, exposure to persistent organic pollutants has been shown to cause immunosuppression in aquatic species (AMAP, 1998; Letcher et al., 2010; Suzuki et al., 2020), and contaminant-induced immunosuppression has been suggested to be a contributing factor to disease-dependent mortality in several marine mammal and fish species infected with various pathogens (Jepson et al., 1999; Ross, 2002; Maule et al., 2005; Arkoosh et al., 2010; Rehberger et al., 2017; Desforges et al., 2018). Likewise, changes of ambient temperature are known to influence the immune system particularly of ectothermic aquatic organisms, what has been shown to lead to altered defense capacity against infectious pathogens [e.g., (Bailey et al., 2017; Traylor-Knowles and Connelly, 2017)]. Overall, there exists strong evidence that man-made stressors, alone or in combination, can compromise the resistance of aquatic organisms to pathogens, thereby contributing to the emergence of infectious diseases. For a better understanding of the relation between environmental change and disease, it is essential to provide knowledge if, and how, the immune system of aquatic organisms responds to multiple stressor exposure, and if and how this translates into an increased occurrence and severity of infectious diseases.

The present Research Topic aims to advance our understanding of the avenue from environmental change (driver) to altered immunity (mechanism) resulting in modified health or disease (outcome) of aquatic organisms. The contributions to the Research Topic shed spotlights on the continuum from environmental stress via immunity to disease. The contribution of Nardi et al. focuses on the interactive effects of environmental stressors – more specifically, temperature change and cadmium exposure -, on the immune system of an aquatic species, the Mediterranean mussel Mytilus galloprovincialis. Currently, there exists no systematic understanding how organisms respond to combinations of stressors of different quality and intensity, i.e. if the stressors act antagonistically, additively, or synergistically. Hence, it is important to broaden our knowledge base on this subject. Bivalves are well-suited study organisms for this type of research, as they are important indicator species for environmental and anthropogenic stressors. The findings of Nardi et al. suggest that the concomitant occurrence of thermal stress and toxic metal stress could elicit interactive and negative effects on the immune system of Mytilus galloprovincialis.

The work by Krasnov et al. investigates two important aspects of the role of environmental stressors in the causation of disease. Firstly, the authors examine the impact of hypoxia on the immune system of Atlantic salmon (Salmo salar) during development. During ontogeny, immune structures and functions experience major modifications, and these changes in the endogenous factors may modulate the immune response to exogenous factors. While this fact is rather basic, its importance for assessing environmental impact on immunity and disease of aquatic organisms is often missed. Secondly, Krasnov et al. evaluate whether the stressor-induced alterations of immune parameters translate into an altered immunocompetence of salmon against pathogens. The complexity of the immune system makes it challenging to select appropriate exposure and effect parameters, and to evaluate the significance of the selected parameters for the overall fitness and immune competence of the organism. Measured parameters may not influence the outcome of infection, and more importantly, adverse effects of stressors may only be detectable after immune system activation, and not in the resting immune system of a noninfected host. The findings of Krasnov et al. provide evidence that hypoxia at early life stages induced sustained effects on the immune system with increased expression of immune genes and attenuation of their downregulation during smoltification. However, these changes did not improve survival of fish after challenge with Moritella viscosa.

The contributions of Ling et al. as well as McCracken et al. attract attention to another often neglected aspect in the linkage between environmental stress, immunity and disease: the role of the microbiome. The microbiome is susceptible to environmental change, and it influences the immune and health status of the host organisms. This intimate relationship provides avenues through which environmental impacts on microbiome homeostasis directly or indirectly may cause disease. McCracken et al. provides an example, where microbial dysbiosis, i.e. changes in the microbiome community composition, preceded signs of sea star wasting disease in wild populations of Pycnopodia helianthoides. Microbiome composition was also shown to be vital in the health of brown seaweed Saccharina japonica, where Ling et al. found that the epimicrobiome shifted with progression of the seaweed bleaching disease.

The two concluding contributions of this Research Topic focus on the ecological implications of environmentally induced disease of aquatic species. Salazar-Forero et al. highlight how strongly pathogen and disease dynamics in wild populations depend on environmental conditions. The authors show that winter storms strongly affected pathogen dynamics with significant pathogen increments in the sea urchin species Diadema africanum and Paracentrotus lividus. Hence, the driver underlying the recurrent pathogen-induced sea urchin mass mortalities in the Canary Islands appears to be the changes of the environmental weather conditions. Tallam and White, finally, suggest to use disease parameters as universal indicators of estuary ecological status or health. The advantage of the disease parameter is that it provides an integrative indicator of ecosystem health rather than a stressor-by-stressor assessment. As already pointed out by Segner et al. (2014), the issue that matters is how the biological or ecological receptors respond to the combined presence of the anthropogenic stressors. Tallam and White have reviewed 22 years of literature. They found that as indicators of both general ecosystem health and of multiple other stressors, diseases play a disproportionally significant role in the face of climate- and anthropogenic-related stressors. While the review focused on estuaries, it is likely that disease is a valuable indicator to assess the health of other ecosystems as well, providing essential markers that should be monitored and modelled further.

Author contributions

AL: Conceptualization, Project administration, Writing – original draft, Writing – review & editing. EH: Conceptualization, Writing – review & editing. HS: Conceptualization, Writing – review & editing.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

References

Adlard R. D., Miller T. L., Smit N. J. (2015). The butterfly effect: parasite diversity, environment, and emerging disease in aquatic wildlife. Trends Parasitol. 31 (4), 160–166. doi: 10.1016/j.pt.2014.11.001

PubMed Abstract | CrossRef Full Text | Google Scholar

AMAP (1998). “AMAP assessment report: Arctic pollution issues,” in Arctic Monitoring and Assessment Programme (AMAP) (Oslo, Norway: Arctic Monitoring and Assessment Programme (AMAP)), 859 pp. Available at: https://www.amap.no/documents/doc/amap-assessment-report-arctic-pollution-issues/68.

Google Scholar

Arkoosh M. R., Boylen D., Dietrich J., Anulacion B. F., Bravo C. F., Johnson L. L., et al. (2010). Disease susceptibility of salmon exposed to polybrominated diphenyl ethers (PBDEs). Aquat. Toxicol. 98 (1), 51–59. doi: 10.1016/j.aquatox.2010.01.013

PubMed Abstract | CrossRef Full Text | Google Scholar

Bailey C., Segner H., Casanova-Nakayama A., Wahli T. (2017). Who needs the hotspot? The effect of temperature on the fish host immune response to Tetracapsuloides bryosalmonae the causative agent of proliferative kidney disease. Fish Shellfish Immunol. 63, 424–437. doi: 10.1016/j.fsi.2017.02.039

PubMed Abstract | CrossRef Full Text | Google Scholar

Bijma J., Pörtner H.-O., Yesson C., Rogers A. D. (2013). Climate change and the oceans–What does the future hold? Mar. Pollut. Bull. 74 (2), 495–505. doi: 10.1016/j.marpolbul.2013.07.022

PubMed Abstract | CrossRef Full Text | Google Scholar

Burge C. A., Mark Eakin C., Friedman C. S., Froelich B., Hershberger P. K., Hofmann E. E., et al. (2014). Climate change influences on marine infectious diseases: implications for management and society. Annu. Rev. Mar. Sci. 6, 249–277. doi: 10.1146/annurev-marine-010213-135029

CrossRef Full Text | Google Scholar

Byers J. E. (2021). Marine parasites and disease in the era of global climate change. Annu. Rev. Mar. Sci. 13, 397–420. doi: 10.1146/annurev-marine-031920-100429

CrossRef Full Text | Google Scholar

Ceballos G., Ehrlich P. R., Barnosky A. D., García A., Pringle R. M., Palmer T. M. (2015). Accelerated modern human–induced species losses: Entering the sixth mass extinction. Sci. Adv. 1 (5), e1400253. doi: 10.1126/sciadv.1400253

PubMed Abstract | CrossRef Full Text | Google Scholar

Ceballos G., Ehrlich P. R., Dirzo R. (2017). Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. Proc. Natl. Acad. Sci. 114 (30), E6089–E6096. doi: 10.1073/pnas.1704949114

CrossRef Full Text | Google Scholar

Chislock M. F., Doster E., Zitomer R. A., Wilson A. E. (2013). Eutrophication: causes, consequences, and controls in aquatic ecosystems. Nat. Educ. Knowledge 4 (4), 10.

Google Scholar

Crain C. M., Kroeker K., Halpern B. S. (2008). Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11 (12), 1304–1315. doi: 10.1111/j.1461-0248.2008.01253.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Desforges J.-P., Hall A., McConnell B., Rosing-Asvid A., Barber J. L., Brownlow A., et al. (2018). Predicting global killer whale population collapse from PCB pollution. Science 361 (6409), 1373–1376. doi: 10.1126/science.aat1953

PubMed Abstract | CrossRef Full Text | Google Scholar

Groh K., Vom Berg C., Schirmer K., Tlili A. (2022). Anthropogenic chemicals as underestimated drivers of biodiversity loss: scientific and societal implications. Environ. Sci. Technol. 56 (2), 707–710. doi: 10.1021/acs.est.1c08399

PubMed Abstract | CrossRef Full Text | Google Scholar

Hutson K. S., Davidson I. C., Bennett J., Poulin R., Cahill P. L. (2023). Assigning cause for emerging diseases of aquatic organisms. Trends Microbiol. 31 (7), 681–691. doi: 10.1016/j.tim.2023.01.012

PubMed Abstract | CrossRef Full Text | Google Scholar

IPCC (2014). Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Eds. Core Writing Team, Pachauri R. K., Meyer L. A. (Geneva, Switzerland: IPCC), 151 pp. Available at: http://hdl.handle.net/10013/epic.45156.d001.

Google Scholar

Jackson J. B., Kirby M. X., Berger W. H., Bjorndal K. A., Botsford L. W., Bourque B. J., et al. (2001). Historical overfishing and the recent collapse of coastal ecosystems. Science 293 (5530), 629–637. doi: 10.1126/science.1059199

PubMed Abstract | CrossRef Full Text | Google Scholar

Jacobson K. C., Arkoosh M. R., Kagley A. N., Clemons E. R., Collier T. K., Casillas E. (2003). Cumulative effects of natural and anthropogenic stress on immune function and disease resistance in juvenile Chinook salmon. J. Aquat. Anim. Health 15 (1), 1–12. doi: 10.1577/1548-8667(2003)015%3C0001:CEONAA%3E2.0.CO;2

CrossRef Full Text | Google Scholar

Jepson P. D., Bennett P. M., Allchin C. R., Law R. J., Kuiken T., Baker J. R., et al. (1999). Investigating potential associations between chronic exposure to polychlorinated biphenyls and infectious disease mortality in harbour porpoises from England and Wales. Sci. Total Environ. 243, 339–348. doi: 10.1016/S0048-9697(99)00417-9

PubMed Abstract | CrossRef Full Text | Google Scholar

Johnson P. T., Paull S. H. (2011). The ecology and emergence of diseases in fresh waters. Freshw. Biol. 56 (4), 638–657. doi: 10.1111/j.1365-2427.2010.02546.x

CrossRef Full Text | Google Scholar

Letcher R. J., Bustnes J. O., Dietz R., Jenssen B. M., Jørgensen E. H., Sonne C., et al. (2010). Exposure and effects assessment of persistent organohalogen contaminants in Arctic wildlife and fish. Sci. Total Environ. 408 (15), 2995–3043. doi: 10.1016/j.scitotenv.2009.10.038

PubMed Abstract | CrossRef Full Text | Google Scholar

Martin L. B., Hopkins W. A., Mydlarz L. D., Rohr J. R. (2010). The effects of anthropogenic global changes on immune functions and disease resistance. Ann. New York Acad. Sci. 1195 (1), 129–148. doi: 10.1111/j.1749-6632.2010.05454.x

CrossRef Full Text | Google Scholar

Maule A. G., Jørgensen E. H., Vijayan M. M., Killie J. E. A. (2005). Aroclor 1254 exposure reduces disease resistance and innate immune responses in fasted Arctic charr. Environ. Toxicol. Chem. 24 (1), 117–124. doi: 10.1897/03-700.1

PubMed Abstract | CrossRef Full Text | Google Scholar

Miller K. M., Teffer A., Tucker S., Li S., Schulze A. D., Trudel M., et al. (2014). Infectious disease, shifting climates, and opportunistic predators: cumulative factors potentially impacting wild salmon declines. Evolutionary Appl. 7 (7), 812–855. doi: 10.1111/eva.12164

CrossRef Full Text | Google Scholar

Palmer C. V. (2018). Immunity and the coral crisis. Commun. Biol. 1, 91. doi: 10.1038/s42003-018-0097-4

PubMed Abstract | CrossRef Full Text | Google Scholar

Rehberger K., Werner I., Hitzfeld B., Segner H., Baumann L. (2017). 20 Years of fish immunotoxicology–what we know and where we are. Crit. Rev. Toxicol. 47 (6), 516–542. doi: 10.1080/10408444.2017.1288024

CrossRef Full Text | Google Scholar

Rohr J. R., Cohen J. M. (2020). Understanding how temperature shifts could impact infectious disease. PloS Biol. 18 (11), e3000938. doi: 10.1371/journal.pbio.3000938

PubMed Abstract | CrossRef Full Text | Google Scholar

Rollins-Smith L. A. (2017). Amphibian immunity–stress, disease, and climate change. Dev. Comp. Immunol. 66, 111–119. doi: 10.1016/j.dci.2016.07.002

PubMed Abstract | CrossRef Full Text | Google Scholar

Ross P. S. (2002). The role of immunotoxic environmental contaminants in facilitating the emergence of infectious diseases in marine mammals. Hum. Ecol. Risk Assessment: Int. J. 8 (2), 277–292. doi: 10.1080/20028091056917

CrossRef Full Text | Google Scholar

Segner H., Schmitt-Jansen M., Sabater S. (2014). Assessing the impact of multiple stressors on aquatic biota: the receptor’s side matters. Environ. Sci. Technol. 48 (14), 7690–7696. doi: 10.1021/es405082t

PubMed Abstract | CrossRef Full Text | Google Scholar

Shears N. T., Ross P. M. (2010). Toxic cascades: multiple anthropogenic stressors have complex and unanticipated interactive effects on temperate reefs. Ecol. Lett. 13 (9), 1149–1159. doi: 10.1111/j.1461-0248.2010.01512.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Suzuki T., Hidaka T., Kumagai Y., Yamamoto M. (2020). Environmental pollutants and the immune response. Nat. Immunol. 21 (12), 1486–1495. doi: 10.1038/s41590-020-0802-6

PubMed Abstract | CrossRef Full Text | Google Scholar

Traylor-Knowles N., Connelly M. T. (2017). What is currently known about the effects of climate change on the coral immune response. Curr. Climate Change Rep. 3, 252–260. doi: 10.1007/s40641-017-0077-7

CrossRef Full Text | Google Scholar

USGCRP (2017). Climate Science Special Report: Fourth National Climate Assessment, Vol I. Eds. Wuebbles D. J., Fahey D. W., Hibbard K. A., Dokken D. J., Stewart B. C., Maycock T. K. (Washington, DC, USA: U.S. Global Change Research Program). 470 pp.

Google Scholar

Keywords: anthropogenic stressors, pollution, climate change, cumulative impacts, immunity, disease resistance and tolerance, infection

Citation: Larsen AK, Holen E and Segner H (2023) Editorial: Immunity and disease of aquatic organisms under the combined impact of anthropogenic stressors: mechanisms and disease outcomes. Front. Mar. Sci. 10:1291639. doi: 10.3389/fmars.2023.1291639

Received: 09 September 2023; Accepted: 13 September 2023;
Published: 22 September 2023.

Edited and Reviewed by:

Christopher Edward Cornwall, Victoria University of Wellington, New Zealand

Copyright © 2023 Larsen, Holen and Segner. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Anett Kristin Larsen, YW5ldHQuay5sYXJzZW5AdWl0Lm5v

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.