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Impact and Range Extension of Invasive Foraminifera in the NW Mediterranean Sea

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Impact and Range Extension of Invasive Foraminifera in the NW Mediterranean Sea Impact and Range Extension of Invasive Foraminifera in the NW Mediterranean Sea Implications for Diversity and Ecosystem Functioning Dissertation zur Erlangung des Doktorgrades (Dr. rer. nat) der Mathematisch-Naturwissenschaftlichen Fakultät der Rheinischen Friedrich-Wilhelms-Universität Bonn vorgelegt von Gloria Hortense Mouanga aus Halle/Saale Bonn, Mai 2017 Angefertigt mit Genehmigung der Mathematisch-Naturwissenschaftlichen Fakultät der Rheinischen Friedrich-Wilhelms-Universität Bonn 1. Gutachter: Prof. Dr. Martin R. Langer 2. Gutachter: Prof. Dr. Jes Rust Tag der Promotion: 27.07.2017 Erscheinungsjahr: 2018 Rheinische Friedrich-Wilhelms-Universität Bonn Bonn, den 09.05.2017 Steinmann Institut Bereich Paläontologie Nussallee 8 53115 Bonn Gloria Hortense Mouanga (MSc.) Erklärung Hiermit erkläre ich an Eides statt, dass ich für meine Promotion keine anderen als die angegebenen Hilfsmittel benutzt habe, und dass die inhaltlich und wörtlich aus anderen Werken entnommenen Stellen und Zitate als solche gekennzeichnet sind Gloria Hortense Mouanga Abstract Climate warming and the poleward widening of the tropical belt have induced range shifts in a variety of marine and terrestrial organisms. Among the key taxa that are rapidly expanding their latitudinal range are larger symbiont-bearing foraminifera of the genus Amphistegina. Amphisteginid foraminifera are abundant in tropical and subtropical reef and shelf regions of the world’s oceans. As key carbonate producers, amphisteginids contribute significantly to carbonate substrate stability, growth of reefal structures, and habitat formation. The Mediterranean Sea represents the northernmost geographical extension of amphisteginid foraminifera. Fueled by substantial warming, the Mediterranean has been identified as one of the most severely affected areas. Analyses of foraminiferal faunas from new sites from the Ionian and Adriatic Sea show that amphisteginid foraminifera continue to expand their biogeographic range, rapidly outcompete all native species and represent the most abundant taxon at almost every site colonized. This study documents for the first time that amphisteginid foraminifera have now crossed the Strait of Otranto and invaded the eastern Adriatic coast along southern Albania. Sampling on the opposite side along the southern part of the Italian boot shows, however, that amphisteginid foraminifera have not yet colonized the western coast of the Adriatic. The asymmetric invasion of the Adriatic displays spatial heterogeneity, where the progressive colonization follows the major surface currents with a northerly flow along the eastern coast and a southerly return along the western coastline. The observed recent rate of range expansion in Amphistegina is computed between 4.0 and 10 km/year-1 and provides strong support for current species model projections. Based on the new data, the range boundary shift is projected to lead to a total northward range expansion of 5.2° latitude in the year 2100. The latitudinal range extension computed for the Mediterranean is thus almost twice as large as those computed for the southern hemisphere. The introduction and range expansion of Amphistegina puts significant pressure on local species, affects foraminiferal diversity and decreases species richness of associated biotas. Native species richness is reduced at all sites invaded by amphisteginids and correlates with the degree of infestation. Amphisteginids invasions specifically impact those species that share a similar microhabitat and include other larger symbiont-bearing foraminifera and numerous trochospiral species. The impact of Amphistegina on native biotas gradually increases from the range expansion front towards those sites where invasions commenced decades ago. High abundances may result in prolific monocultures of Amphistegina that modify the composition of sedimentary substrates and ultimately trigger changes in ecosystem functioning. Assemblage structures and patterns observed at the expansion front in modern- day environments resemble amphisteginid invasions recorded in Miocene foraminiferal communities from the Vienna Basin and Poland. Miocene range shifts are among the largest biogeographic range expansions documented in earth history and highlight the magnitude of modern ocean range shifts. The ongoing range extension into new areas of the Mediterranean Sea is shown to trigger changes in community structures with potential consequences for ecosystem functioning. Numerical abundances and impacts of invasive amphisteginids are greatest at shallow depths <20 m. Evidence is now accumulating that the invasion of amphisteginid foraminifera results in (1) a loss of benthic foraminiferal biodiversity, (2) alterations of foraminiferal community structures and (3) shifts in abundances of functional groups of foraminifera. iv For comparison, benthic foraminiferal assemblages in human impacted and non-impacted areas were studied (also partly inhabited by amphisteginids). The study area is the seacoast of Albania, located along the north-eastern Ionian and southeastern Adriatic Sea. Its shallow waters provide a wide range of habitats for a large number of marine species. The composition and distribution of shallow-water benthic foraminiferal assemblages in relation to substrates, water depth and ecological conditions were documented. The samples collected show high species richness values (277 species, 112 Genera) with taxa known to be distributed in the Adriatic as well as in the eastern and western Mediterranean Sea. The performed hierarchical cluster analysis reveals the presence of two distinct clusters and biofacies characterized for the northern and southern coastline respectively. Increasing anthropogenic pressure accompanied with pollution from sewage, urban wastes, maritime traffic, and building activities lead to partly degrading conditions in the Gulf of Vlore and Sarande Bay. Darezeze e Re, Shengjin, Durres, and Divjaka show likewise increasing degradation rates traced back to human mediated impacts (urban and industrial sewages, hydrocarbon exploration, building activities) and natural forcing (river discharge, erosion rates). The presence of non-indigenous (NI) benthic foraminifera with Indo-Pacific origin in the samples sites off Albania is documented. The presence of NI benthic foraminiferal species of Indo-Pacific and Atlantic origin is mainly controlled by rising sea surface temperatures and the subsequent dispersal by currents. Ballast ship water is also considered to be a major source of non- native species introductions. The invasive benthic foraminifera Amphistegina lobifera is currently the most abundant species, which continues to proliferate along the Albanian coastline with severe consequences on native biotas and ecosystem functioning. v Zusammenfassung Klimaerwärmung und die Erweiterung des tropischen Gürtels in Richtung der Polregionen führt zur Ausbreitung vieler mariner und terrestrischer Organismen. Zu den Taxa, die ihr Verbreiterungsareal um mehrere Längengrade erweitern, gehören symbionten-tragende Foraminiferen der Gattung Amphistegina. Amphisteginen sind besonders häufig in tropischen und subtropischen Riffen und Schelfmeeren der Welt. Als Schlüsselproduzenten für Karbonat tragen sie erheblich zur Stabilität von karbonatischen Substraten, dem Wachstum von Riffstrukturen und Habitaten bei. Das Mittelmeer bildet die nördlichste geographische Erweiterung amphisteginer Foraminiferen. Das Mittelmeer gehört, angetrieben von der erheblichen (Klima)Erwärmung, zu den am schlimmsten betroffenen Gebieten der Welt. Analysen der Foraminiferenfauna von neuen Standorten innerhalb des Ionischen und Adriatischen Meeres zeigen, dass Amphisteginen kontinuierlich ihre biogeographische Ausdehnung erweitern und rapide native/heimische Arten auskonkurrieren und das häufigste Taxon in nahezu allen Bereichen bildet, die sie kolonisiert. Diese Studie dokumentiert zum ersten Mal, dass Amphisteginen nun die Straße von Otranto passiert haben und die östliche Adria entlang der südlichen albanischen Küste besiedeln. Die Probennahmen auf der gegenüberliegenden Seite, entlang des südlichen Teils des italienischen Stiefelabsatzes zeigen, dass Amphisteginen noch nicht die südwestliche Küste der Adria besiedelt haben. Die asymmetrische Besiedelung der Adria zeigt, dass die progressive Kolonisierung der oberflächlichen Meeresströmung folgt, welche entlang der östlichen Adriaküste nach Norden verläuft und in der nördlichen Adria abbiegt und entlang der Westküste nach Süden fließt. Die Ausbreitungsgeschwindigkeit von Amphistegina wurde auf 4.0 bis 10km/Jahr berechnet und bestätigt gegenwärtige Ausbreitungsmodelle für diese Art. Basierend auf den neuen Daten, wird die zukünftige Arealextension im Jahr 2100 auf eine latitudinale Ausweitung von 5.2° projektiert. Die latitudinale Ausweitung, die für das Mittelmeer errechnet wurde ist demnach nahezu doppelt so hoch wie die Ausbreitungsmodelle für die südliche Hemisphäre voraussagen. Die Invasion und Ausbreitung von Amphistegina erhöht signifikant den Druck auf die native Fauna, beeinflusst die Diversität der Foraminiferen, und minimiert die Artenvielfalt vergesellschafteter Faunen. Die natürliche Artenvielfalt ist in allen besiedelten Standorten verringert und korreliert mit dem Grad des Befalls. Die Invasion von Amphisteginen beeinträchtigt vor allem die Arten, welche dieselben Mikrohabitate besiedeln, wie andere symbionten-tragenden Foraminiferen und zahlreiche Arten mit trochospiraler Morphologie. Der Einfluss auf die natürliche
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