Leben im globalen Wandel: Anpassungsmechanismen des marinen Dreistachligen Stichlings Gasterosteus aculeatus

Due to ongoing increases in carbon dioxide (CO2) concentrations in the atmosphere, the world’s climate is changing at an unprecedented rate, leading to rising global mean air and water temperatures. When atmospheric CO2 dissolves in seawater, ocean pH declines, causing an acidification of the ocean. These altered environmental conditions are highly probable to have severe impacts on marine organisms by affecting their performance and survival. When environmental stress is increasing, some species can migrate to habitats with more favourable conditions, others have to adapt to changing conditions. Whether species will be able to adapt fast enough to keep pace with changing environments will be one decisive factor for population persistence. In this thesis, a prime model organism, the three-spined stickleback Gasterosteus aculeatus, was used to study ecological and evolutionary effects of rising water temperatures and ocean acidification on marine fish populations. Rising temperatures are likely to stress marine species, dependent on their thermal tolerance. Thermal stress can alter immune functions of organisms, thereby increasing the susceptibility to infectious diseases. By combining the effects of elevated temperature and bacterial infection in a common garden experiment, the influence of thermal stress on evolutionary trajectories of disease resistance in three-spined stickleback populations could be investigated (chapter II). Environmental stress negatively impacted life-history traits and pathogen resistance of sticklebacks. Furthermore, thermal stress reduced genetic differentiation between populations by releasing cryptic within-population variation. While life-history traits showed positive genetic correlations between temperatures and genotype by environment interactions (GxE), thermal stress led to negative genetic correlations in disease resistance, showing that evolutionary responses in altered environments can be hard to predict from prevailing conditions. Rising temperatures, on the other hand, promote the development of many parasites and pathogenic bacteria, increasing the risk of infection and diseases during summer. To understand infection patterns in relation to water temperature, the parasite and bacterial communities of marine fish species were investigated over a period of two years (chapter I). Temporarily elevated water temperatures resulted in increased macroparasite and bacterial diversities in marine fish species. In addition, some parasite groups showed a forward shift and extension in infection peaks, following warmer spring seasons. This shows that even subtle changes in seasonal temperatures can have an effect on the epidemiology and phenology of parasites as well as opportunistic pathogens. Increased virulence of pathogens at higher temperatures in combination with immune-compromised hosts can have far fetching consequences for marine ecosystems. Next to rising ocean temperatures, marine organisms have to cope with ocean acidification. It has been shown, that elevated CO2 concentrations negatively impacted fish development and survival, particularly in early developmental stages. A powerful mechanism to mediate the effects of global change is transgenerational acclimation. By acclimating parents and offspring to different CO2 concentrations, within- and transgenerational effects of ocean acidification on life-history traits of marine sticklebacks were studied (chapter III). Exposure to elevated CO2 concentrations led to an increase in clutch size in adults as well as increased juvenile survival and growth rates. Transgenerational effects could be found for juvenile growth and for otolith characteristics, suggesting that parental acclimation can modify ocean acidification effects. To summarize, three-spined sticklebacks cope better with ocean acidification than with rising ocean temperatures. Transgenerational acclimation enables sticklebacks to respond quickly to environmental changes and provides time for genetic evolution, as long-term adaptive mechanism, to catch up. The high tolerance to fluctuations in water chemistry and temperature as well as the substantial amount of standing genetic variation suggest that stickleback populations can adapt fast enough to changing environmental conditions.Durch stetig ansteigende Kohlenstoffdioxid-Konzentrationen (CO2) ändert sich das weltweite Klima mit rasanter Geschwindigkeit und Luft- und Wassertemperaturen steigen. Wenn sich atmosphärisches CO2 im Meerwasser löst, sinkt der pH-Gehalt des Meeres und führt zu einer Versauerung des Ozeans. Diese veränderten Umweltbedingungen können schwerwiegende Folgen für die Leistungsfähigkeit und das Überleben von Meeresbewohner haben. Wenn der Umweltstress ansteigt, können einige Arten in Habitate mit geeigneteren Bedingungen ausweichen, andere wiederum müssen sich an die veränderten Umweltbedingungen anpassen. Ob Lebewesen in der Lage sind, sich schnell genug an die sich ändernde Umwelten anzupassen, wird ein entscheidender Faktor für das Bestehen von Populationen sein. Um ökologische und evolutionäre Effekte des globalen Wandels auf marine Fischpopulationen zu untersuchen, wurde ein hervorragend geeigneter Modellorganismus, der Dreistachlige Stichling Gasterosteus aculeatus, für diese Arbeit verwendet. Abhängig von der thermalen Toleranz, können ansteigende Temperaturen Stress in marinen Lebewesen hervorrufen. Thermaler Stress kann Immunfunktionen von Organismen beeinflussen und dadurch die Anfälligkeit für Infektionskrankheiten erhöhen. Durch die kombinierten Effekte von erhöhter Temperatur und bakterieller Infektion in einem „common garden“ Experiment, konnte der Einfluss von thermalem Stress auf evolutionäre Mechanismen der Pathogenresistenz bei Stichlings-populationen untersucht werden (Kapitel II). Umweltstress beeinträchtigte Fitnesskomponenten und Pathogenresistenzen bei Stichlingen. Zudem führte thermaler Stress zu reduzierter genetischer Differenzierung zwischen Populationen. Während Fitnesskomponenten eine positive genetische Korrelation zwischen Temperaturen zeigten, führte thermaler Stress zu einer negativen genetischen Korrelation für Krankheitsresistenz. Ausgehend von vorherrschenden Bedingungen scheinen evolutionäre Antworten auf veränderte Umwelten schwer vorhersagbar. Ansteigende Temperaturen begünstigen andererseits die Entwicklung von vielen Parasiten und pathogenen Bakterien und erhöhen dadurch das Risiko für Infektionen und Krankheiten während des Sommers. Um temperaturbedingte Infektionsmuster zu verstehen, wurden die Parasiten- und Bakteriengemeinschaften von marinen Fischarten in einem Zeitraum von zwei Jahren untersucht. Kurzzeitig ansteigende Wassertemperaturen verursachten erhöhte Makroparasiten- und Bakteriendiversitäten in marinen Fischarten. Zusätzlich zeigten einige Parasitengruppen eine Verschiebung und Ausdehnung des Infektionshöhepunkts durch wärmere Frühlingsmonate. Bereits kleine Änderungen in saisonalen Temperaturen können die Epidemiologie und die Phänologie von Parasiten, als auch von opportunistischen Pathogenen, beeinflussen. Erhöhte Pathogenvirulenz durch ansteigende Temperaturen kombiniert mit immungeschwächten Wirten kann zu weitreichenden Konsequenzen für marine Ökosysteme führen. Neben ansteigenden Wassertemperaturen, müssen marine Lebewesen auch mit Ozeanversauerung umgehen. Es wurde bewiesen, dass erhöhte CO2 Konzentrationen die Entwicklung und das Überleben von Fischen beeinträchtigt. Ein wirkungsvoller Mechanismus, um die Effekte des globalen Wandels zu mildern, ist transgenerationale Akklimatisierung. Durch das Akklimatisieren von Eltern und Nachwuchs an verschiedene CO2 - Konzentrationen, konnten inner- und trans-generationale Effekte von Ozeanversauerung auf marine Stichlinge untersucht werden (Kapitel III). Erhöhte CO2 - Konzentrationen führten zu vergrößerten Eigelegen bei den Eltern, als auch zu erhöhten Überlebens- und Wachstumsraten bei den Juvenilen. Transgenerationale Effekte konnten für juveniles Wachstum und für Otolithencharakteristiken bestätigt werden und lassen darauf schließen, dass elterliche Akklimatisierung die Auswirkungen von Ozeanversauerung verändern können. Zusammenfassend ist zu erwähnen, dass der Dreistachlige Stichling mit Ozeanversauerung besser umgehen kann, als mit ansteigenden Meerestemperaturen. Zudem ermöglicht transgenerationale Akklimatisierung, Stichlingen auf Umweltveränderungen schnell zu reagieren, bevor genetische Evolution, als Langzeitanpassungsmechanismus, übergreift. Die hohe Toleranz für schwankende Wasserchemie und Temperatur, als auch die erhebliche Menge an dauerhafter genetischer Varianz ermöglicht Stichlingspopulationen sich schnell genug an die sich verändernde Umweltbedingungen anzupassen

Living apart together: Long-term coexistence of Baltic cod stocks associated with depth-specific habitat use

Coexistence of fish populations (= stocks) of the same species is a common phenomenon. In the Baltic Sea, two genetically divergent stocks of Atlantic cod (Gadus morhua), Western Baltic cod (WBC) and Eastern Baltic cod (EBC), coexist in the Arkona Sea. Although the relative proportions of WBC and EBC in this area are considered in the current stock assessments, the mixing dynamics and ecological mechanisms underlying coexistence are not well understood. In this study, a genetically validated otolith shape analysis was used to develop the most comprehensive time series of annual stock mixing data (1977–2019) for WBC and EBC. Spatio-temporal mixing analysis confirmed that the two stocks coexist in the Arkona Sea, albeit with fluctuating mixing proportions over the 43-year observation period. Depth-stratified analysis revealed a strong correlation between capture depth and stock mixing patterns, with high proportions of WBC in shallower waters (48–61% in <20m) and increasing proportions of EBC in deeper waters (50–86% in 40-70m). Consistent depth-specific mixing patterns indicate stable differences in depth distribution and habitat use of WBC and EBC that may thus underlie the long-term coexistence of the two stocks in the Arkona Sea. These differences were also reflected in significantly different proportions of WBC and EBC in fisheries applying passive gears in shallower waters (more WBC) and active gears in deeper waters (more EBC). This highlights the potential for fishing gear-specific exploitation of different stocks, and calls for stronger consideration of capture depth and gear type in stock assessments. This novel evidence provides the basis for improved approaches to research, monitoring and management of Baltic cod stocks

Proportion of WBC in SD 24.

Mixing proportions are based on cod samples from 1st and 4th quarter trawl surveys between 1995 and 2016 (selected years, NOtoliths = 7532). Absolute numbers of otoliths used in the shape analysis are given on the top of each bar. (TIF)</p

Spatial distribution of annual stock mixing proportions in SD 24.

Mixing proportions of WBC (blue) and EBC (red) are based on cod samples (N = 6597) from trawl surveys between 2010 and 2019, grouped by ICES rectangles (see Fig 1 for statistical rectangles). Rectangles are arranged according to their relative position within SD 24 from west to east and from north to south (Fig 1). Absolute numbers of otoliths used in the shape analysis are given on the right side of each year. Years without bars = no data available. (TIF)</p

Sampling locations of Baltic cod in SD 24 separated by sampling decade.

Cod samples originate from bottom-trawl survey catches between 1977 and 2019. (TIF)</p

Seasonal proportions of WBC in SD 24.

Mixing proportions are based on cod samples from German commercial catches between 2010 and 2019 (selected years, NOtoliths = 10 924). Active and passive gear samples are pooled. Absolute numbers of otoliths used in the shape analysis are given on the top of each bar. Quarters without bars = no data available. (TIF)</p

GLMs containing stock mixing proportions of survey and commercial data as Gaussian response variable and mean depth, longitude, latitude and capture year of fishing hauls as predictors.

GLMs containing stock mixing proportions of survey and commercial data as Gaussian response variable and mean depth, longitude, latitude and capture year of fishing hauls as predictors.</p

Summary of cod samples from German trawl survey catches in SD 24 between 1977 and 2019.

Table comprises sampling year and months, sample size (N), sampled areas (A = 12°-13° E, B = 13°-14° E, C = 14°-15° E), total fish length (range and mean ± SD (standard deviation)), proportion of spawning individuals (maturity stage 5 and 6, following [10]) and proportion of female fish. *These samples were used only for the comparison of mixing proportions between quarters within the same year. (DOCX)</p

Annual mixing proportions of the Baltic cod stocks in SD 24.

Mixing proportions of WBC (blue) and EBC (red) are based on cod samples (N = 20 302) from trawl surveys between 1977 and 2019. Total numbers of fishing hauls used in the stock mixing analysis (in brackets) and absolute numbers of otoliths used in the shape analysis (in bold) are given on the right side of each year. Years without bars = no data available.</p