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Effects of environmental stress on early life history stages of the European shore crab Carcinus maenas Linnaeus 1758 (Brachyura: Portunidae)

  • Climate change threatens marine ecosystems by simultaneous alterations and fluctuations in several abiotic factors like temperature, salinity and pH. Therefore, a strong ability to cope with varying environmental factors is indispensable for marine organisms. Especially, larvae of meroplanktonic species will be affected by predicted alterations in environmental conditions as planktonic larval stages are considered the most sensitive stages during life history (Anger 2001). The European shore crab Carcinus maenas, as an ecological key species, was chosen as a model species to investigate multiple stressor effects on early life history stages of marine meroplanktonic invertebrates. The life cycle of C. maenas is biphasic consisting of five pelagic larval stages (four zoeal and one megalopal stage), followed by benthic juvenile and adult phases. The metamorphic molt from the last zoeal stage to the semi-benthic Megalopa includes dramatic changes in ecology, habitat, behavior, feeding, morphology, and physiology. During life history, zoeal stages of C. maenas are of particular interest in the course of climate change as these stages are more vulnerable than the following developmental stages to alterations in abiotic factors. The aim of the present thesis was to develop an integrative view on effects of long-term exposure, from hatching to metamorphosis, to increased temperature and hypo-osmotic conditions on early life history stages of C. maenas. We wanted to gain insights into larval responses to climate driven environmental variables, more specifically, on how tolerance to low salinity is affected by increased temperatures. Consequently, the present study investigated the effect of long-term exposure to twelve different sub-lethal temperature and salinity combinations in an ecological relevant range on larval development of C. maenas. In a multidisciplinary approach, larval responses in performance (survival and developmental duration) and morphology were measured. Furthermore, analysis on larval ontogeny and organogenesis created the foundation for analysis of larval response to multiple stressors in anatomy. Results of the present thesis demonstrated that despite their different life-styles and external morphology, brachyuran larvae are smaller versions of their adults when regarding their inner organization: the adult bauplan unfolds from organ anlagen compressed into miniature organisms. In addition, they provide an overall picture of seemingly gradual organogenesis across larval development and the metamorphic molt, an insight that contrasts with the abrupt external morphological changes during metamorphosis. Gradual anatomical changes in e.g. osmoregulatory structures like gills and antennal glands allowed for ontogenetic shifts of tolerance to temperature and salinity during zoeal development and successive increase in osmo- and thermoregulatory capability. On the other hand, osmoregulatory structures as seen for adults were underdeveloped during zoeal development and therefore do not qualify for osmoregulatory function for these stages. This potentially explains the higher sensitivity of zoeae to hypo-osmotic conditions. Early life history stages of C. maenas were affected on all response levels by the tested multiple stressors. The interaction of temperature and salinity was of antagonistic type, resulting in general reduced stress for larval stages. Nevertheless, low salinity had a strong negative impact on survival, while increased temperature caused ann acceleration of development. Furthermore, the size of zoeae of C. maenas was driven by the interaction of temperature and salinity, with extreme conditions, causing diminished growth, thus resulting in smaller larval size. On the other hand, larval shape was only slightly affected by changes of abiotic factors. Volume of the digestive gland and the heart of larvae from long-term exposure to sub-lethal temperatures and salinities showed high variability. Larval responses were affected by the stressors intensities: moderately high temperatures lessened the negative effects of low salinities, while extreme high temperatures exceeded the ameliorating effect of temperature on stressful salinity conditions. On the other hand, the tolerance to temperature and salinity increased during larval development indicating an ontogenetic shift in response to multiple stressors with development. In addition, performance, morphology, and multiple stressor interaction showed intrapopulation variability among larvae hatched from different females, and between experimental periods. In conclusion, this study highlighted direct effects of abiotic factors on all investigated response levels in early life history stages of the meroplanktonic larvae of the invertebrate C. maenas. High mortality rates combined with higher sensitivity confirm that planktonic early life history stages are the bottleneck during life history of this species. Nevertheless, early life history stages of C. maenas had the ability to cope with wide ranges of changing environmental factors. The antagonism between temperature and salinity on larval development offers potential for early life history stages to persist in a changing world. Furthermore, anatomical structures allow for slight eurytolerance and potentially for compensation of abiotic stress. Overall, slight increases in temperature, driven by climate change may enable larvae of C. maenas to tolerate exposure to moderately low salinities and, combinedwith intrapopulation variability, potentially allows for population persistence. Summarized, this study emphasizes the importance of testing a wide range of ecologically relevant traits in developing pelagic larvae in order to properly characterize their response to environmental change. Changes in abundance and phenology of planktonic larvae like the zoeae of C. maenas have major potential to change a species‘ population structure significantly, and furthermore indirectly affect whole community and ecosystem structures. Therefore, this thesis may serve as a bridge to future studies in evolutionary and ecological developmental biology.
  • Langzeitmessungen zeigen bereits den massiven Einfluss globaler Umweltänderungen auf marine Ökosysteme einschließlich des Planktons. Insbesondere Randmeere wie die Nordsee werden zunehmend von steigender Temperatur betroffen sein. Zusätzlich zur Temperatur ändern sich weitere Faktoren wie beispielsweise Salinität und pH. Diese gleichzeitige Änderung zahlreicher Faktoren zwingt marine Organismen mit der Instabilität ihrer Umgebung umzugehen. Planktonische Larven mariner benthischer Organismen spielen eine zentral Rolle in der Beständigkeit deren Populationen und der Verbreitung einer Art. Gleichzeitig sind Larven das empfindlichste Entwicklungsstadium und daher extrem von sich ändernden Umweltbedingungen beeinflusst. Daher ist es wichtig, die Reaktion dieser Larven auf Änderungen abiotischer Faktoren wie Temperatur und Salinität zu quantifizieren, um die Beständigkeit einer Art in einem sich ändernden Ökosystem abzuschätzen. Dieses Projekt hat zum Ziel, larvale Merkmale am der gemeinen Strandkrabbe Carcinus maenas zu identifizieren, welche von der Kombination aus Temperatur- und Salinitätsstress beeinflusst sind. Dafür wurde die larvale Performance (Überleben und Entwicklungsdauer) unter zwölf verschiedenen Temperatur-Salinitäts-Kombinationen verglichen und die Variation innerhalb einer Population untersucht. Des Weiteren wurde die äußere und innere Morphologie der Larven vergleichend untersucht. Es zeigte sich, dass die Interaktion von Temperatur und Salinität sowohl Überleben als auch Entwicklungsdauer beeinflusst. Die Interaktion erhöhter Temperatur und niedriger Salinität selbst ist antagonistisch; im Zuge dessen verbessert erhöhte Temperatur den negativen Effekt niedriger Salinität. Des Weiteren wurde eine hohe intraspezifische Variation in der Auswirkung abiotischer Faktoren und entsprechend der larvalen Performance festgestellt. Es konnte keine Auswirkung der getesteten Faktoren auf die äußere Morphologie der Larven festgestellt werden. Die Untersuchung der larvalen Organogenese ergab eine graduelle Zunahme in der Größe und Komplexität der einzelnen Organsysteme; die meisten Organe erwachsener Krabben sind bereits in Larvenstadien als Anlagen vorhanden. Massive Lipidinklusionen der Mitteldarmdrüse als Zeichen des Ernährungszustandes erlauben potentiell für die Kompensation erhöhter metabolischer Kosten verursacht durch stressige Umweltbedingungen. Zudem wurde eine vermeintlich funktionelle Antennaldrüse identifiziert, welche in erwachsenen Stadien an der Ionenregulation beteiligt ist und es den Larven unter Umständen erlaubt mit Änderungen der umgebenden Salinität zurechtzukommen. Alles in Allem, könnte die Erwärmung der Meere entsprechend die weitere Ausbreitung von Carcinus maenas in Bereich niedrigerer Salinität durch die antagonistische Interaktion zwischen Temperatur und Salinität und morphologische Anlagen der Larven begünstigen.

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Metadaten
Author: Franziska Spitzner
URN:urn:nbn:de:gbv:9-opus-24969
Title Additional (German):Untersuchung der Auswirkung umweltbedingten Stresses auf frühe Entwicklungsstadien der Europäischen Strandkrabbe Carcinus maenas Linnaeus 1758 (Brachyura: Portunidae)
Referee:Prof. Dr. Steffen Harzsch, Prof. Dr. Maarten Boersma
Advisor:Prof. Dr. Steffen Harzsch
Document Type:Doctoral Thesis
Language:English
Year of Completion:2019
Date of first Publication:2019/02/06
Granting Institution:Universität Greifswald, Mathematisch-Naturwissenschaftliche Fakultät
Date of final exam:2018/11/29
Release Date:2019/02/06
GND Keyword:Carcinus maenas, Klimaänderung, Larvalentwicklung
Pagenumber:187
Faculties:Mathematisch-Naturwissenschaftliche Fakultät / Zoologisches Institut und Museum
DDC class:500 Naturwissenschaften und Mathematik / 500 Naturwissenschaften