The most invasive benthic foraminifera in the Mediterranean Sea

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with up to3.75g tests/5 g sediment and more (Meric et al. 2008a). Macro- and microhabitats former inhabited by native epifauna, especially around Israel and Turkey are now occupied by alien and cryptogenic species.

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Fig. 6 (A) Biogeographic distribution of Amphisorus hemprichii in the Mediterranean and Red Sea, (B) Amphisorus hemprichii population on Halophila stipulacea Ascherson, Kas -Antalya, depth 26 m, scale bar = 6mm (Meric et al. 2014), (C) Amphisorus hemprichii population on Cystoseira sp., Kas - Antalya, depth 12m, scale bar = 2mm (Meric et al. 2014), (D) Amphisorus hemprichii individuals on the sea bottom, scale bar = 0.85, (E) dense A. hemprichii population on hard substrates, serving as a hiding place for a young individual of Octopus vulgaris, scale bar = 6mm (Photo: Baki Yokes; source: Cinar et al. 2010).

1.8.2 Amphistegina spp.

Among the most successful invaders are symbiont-bearing foraminifera of the genus Amphistegina spp., which commonly comprise two species in the Mediterranean, Amphistegina lobifera Larsen, 1976 and Amphistegina lessonii d'Orbigny, 1826 and two ecomorphotypes A. cf. A. lessonii and A. cf.

A. papillosa, although there might be more ecomorphotypes present (Hyams et al. 2002 mentioned biconvex A. lessonii types which may be hard substrate phenotypes and rarely occurring spiro-convex forms, considered to be sandy substrate morphotypes of A. lessonii). Another 3 taxa comprise A.

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radiata, A. papillosa? and A. bicirculata all documented in historical samples from the National History Museum (NHM) in Israel (Benjamini and Almogi-Labin, 2008) and Egypt (Alexandria, Samir and El-Din, 2001, A. radiata). Amphistegina madagascariensis was documented from shallow-waters of Egypt (Samir et al. 2003) and Tunisia (Gulf of Gabes, Blanc-Vernet et al. 1979).

Amphisteginid foraminifera are among the most prolific and ubiquitous foraminifera on coral reefs and tropical carbonate shelves hosting diatom endosymbionts. As key carbonate producers they have often been referred to as living sands (Lee, 1995) and contribute substantially to substrate stability, the growth of reefal structures and the deposition of coastal sediments (McKee et al. 1959; Hallock, 1981;

Langer and Hottinger, 2000; Langer, 2008a, b; Langer et al. 2012, 2013). They are circumtropically distributed, where they thrive in warm, clear, nutrient-poor, carbonate-rich, shallow-shelf environments (Todd, 1976; Hallock, 1988, 1999; Langer and Hottinger, 2000). Amphistegina lobifera, which is the most abundant and successful amphistegnid foraminifera in the Mediterranean, is a major carbonate producer in shallow shelf and reef environments of the tropical realm, precipitating up to 2kg/m²/year (Langer et al. 1997). In the Mediterranean Sea, A. lobifera is listed among the 100 worst invasive species (Zenetos et al. 2005).

The genus Amphistegina occupies a dominating position in many foraminiferal assemblages in tropical realms, particularly in the Pacific, and is found as a common to abundant constituent of foraminiferal faunas in the Cenozoic in both the eastern and western hemisphere (Todd, 1976). In modern oceans, amphisteginid foraminifera have been found as far North as 39° and 31° South displaying some of the widest latitudinal extensions among larger-benthic foraminifera analyzed to date (Langer and Hottinger 2000; Langer, 2008a; Fig. 7F). The Mediterranean Sea represents the northernmost range front of amphisteginids. In the Mediterranean Sea several amphisteginid species are known from Eocene to Pliocene in Amphistegina-rich levels. Amphistegina is the most important rotaliine larger foraminiferal genus which survived the Late Miocene Salinity Crisis attaining a widespread distribution throughout the Mediterranean in Early to Middle Pliocene times (Di Bella et al. 2005).

Concrete data about the paleo-temperature in the Mediterranean are supplied by the presence of the symbiont-bearing foraminifera Amphistegina in the Tyrrhenian Sea, and the absence of Porites reefs (Checconi et al. 2007; Por, 2009). It is assumed (although not proved) that the genus became extinct in the western Mediterranean in Late Pliocene-Early Pleistocene times, whereas it may have survived in the Eastern Mediterranean (Reiss and Hottinger, 1984). Alternatively, it may have re-colonized more recently the Mediterranean along with other larger foraminifera as Lessepsian immigrant from the Indian Ocean (Reiss and Hottinger, 1984). Amphistegina lessonii has been reported from Miocene (e.g Menorca; Mateau-Vicens et al. 2009) and Pleistocene deposits (Parker et al. 2012; Meric et al. 2015) so that it is classified as native Mediterranean species. The examination of historical collections at the NHM for symbiont-bearing foraminifera revealed (among others) the presence of A. lessonii, A.

radiata, A. papillosa (?) and A. bicirculata in material collected from shore sands and dredging taken in the 1850’s off Tunisia, Malta, Italy and Crete (Benjamini and Almogi-Labin, 2008). These foraminifera cannot have entered the Mediterranean via the Suez Canal, suggesting some warm water refugia during the Messinian Salinity Crisis for larger symbiont-bearing species, located on the arch between the Western Mediterranean and Levantine basins (Benjamini and Almogi-Labin, 2008).

Amphistegina madagascariensis has been documented in shallow-waters off Tunisia (Blanc-Vernet et al. 1979) and Egypt (Samir et al 2003) and is considered to be a Lessepsian migrant or introduced via ship ballast water. Amphistegina lobifera has not been reported as early as Pleistocene (Parker et al.

2012) and is therefore classified as a cryptogenic taxon.

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Fig. 7 (A) Biogeographic distribution of Amphistegina spp. in the Mediterranean Sea, Red Sea and the Sea of Marmara. (B) Amphistegina lobifera population on a rock substrate, Üçadalar, Antalya, Mediterranean, 6.00m, scale bar = 20mm (Meric et al. 2014), (C) Amphistegina lobifera population on Cystoseira sp., Bodrum, Mugla, Aegean Sea, 9.00m, scale bar = 15mm (Meric et al. 2014), (D)Amphistegina lobifera population on algal mat, Arsuz, Iskenderun, Hatay, 8.00m, scale bar = 20mm. (Meric et al. 2014), (E) High accumulation rate of A.

lobifera tests in shallow-waters off Cyprus, scale bar = 2mm, (F) global biogeographic distribution of amphisteginid foraminifera ranging from 40°N to 31°S (Weinmann, unpubl. data).

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Amphisteginid foraminifera in the Mediterranean have the greatest spatial distribution among all alien and cryptogenic foraminifera and were locally shown to occur at abundances of up to 350 individuals/g sediment or up to 700 per g dry algae (Gruber et al. 2007; Meric et al. 2008a; Yokes and Meric, 2009). The Mediterranean range expansion front of amphisteginid foraminifera runs from the North African coast off Tunisia to the Pelagian Islands, Malta, the southeastern coast of Sicily and Corfu in northwestern Greece (Yokes et al. 2007; Triantaphyllou et al. 2009, 2012; Zenetos et al.

2010; Langer et al. 2012; Weinmann et al. 2013b; Fig 8A). Amphistegina radiata occurs in moderate percent abundances (0.3-2.9) in shallow-waters of Egpyt (Samir et al. 2001) and is, furthermore, solely documented in the historical samples investigated by Benjamini and Almogi-Labin in 2008.

Amphistegina papillosa? (except of the ecomorphotype A. cf. papillosa) and A. bicirculata (only documented in the NHM historical samples) have never been reported again within the Mediterranean, pointing to an extirpation of these taxa, an established small population in shallow-waters off Tunisia, Malta, Italy and Crete or it is a question of synonymy. Its validity definitely requires further examinations. Amphistegina lobifera and A. lessonii show the greatest spatial distribution among Mediterranean amphisteginids, whereas the two ecomorphotypes A. cf. lessonii and A. cf. papillosa where only described from the Pelagian Islands (Caruso and Cosentino, 2014).

At several sites in the eastern Mediterranean Sea, amphisteginid foraminifera were recently reported to constitute up to 97% of the sediment (Hyams et al. 2002; Gruber et al. 2007; Abu Tair and Langer, 2010; Abu Tair, 2011; Triantaphyllou et al. 2012; Langer et al. 2012; Caruso and Cosentino, 2014; see also Fig. 7E). Like their counterparts in the tropics, amphisteginids in the Mediterranean (especially A.

lobifera) preferentially live on hard substrates covered by macroalgae and algae mats, but are also distributed on carbonate rich coarse to medium grained soft substrates (Hallock, 1981, 1988, 1999;

Hohenegger, 1994; Hohenegger et al. 1999; Renema and Trolestra, 2001). Amphistegina lobifera is the shallowest dwelling of the extant members of the genus thriving in high-energy hydrodynamic conditions (Hallock, 1981; Hallock et al. 1986), where it prefers mid-to high light conditions in 1-5m water depth (Hallock 1981, 1984; Hallock et al. 1986). Although A. lessonii also belongs to the shallow dwelling amphisteginids (generally in 5-20m water depth, Hallock, 1984; Hallock and Hansen, 1979), it seems to be excluded from high energy environments (Hallock, 1984) and can be inhibited by light intensities close to full sunlight (Hallock, 1981). Tropical A. lessonii are also distributed in greater water depth in deep-lagoonal and outer slope settings (Todd, 1976). In the Mediterranean Sea, A. lobifera and A. lessonii, may be found in the same depth range although A.

lessonii is generally also found in greater water depths (>20-70m) and is truncated by the thermocline (16°C) occurring between 60 and 70m (Hollaus and Hottinger, 1997). Considering the abundance and distribution within the Mediterranean, A. lobifera is much more frequent and show a greater spatial distribution than A. lessonii. Whereas A. lobifera becomes dominant and invasive in nearly every habitat colonized, A. lessonii is distributed in shallow waters off Israel (less abundant than A. lobifera;

Hyams et al. 2002), Turkey (rarely distributed; Meric et al. 2010), Egypt (frequently; Parker et al.

2012); Linosa (frequently; Pelagian islands; Caruso and Cosentino, 2014), Greece (frequently; Hollaus and Hottinger, 1997; Triantaphyllou et al. 2003, 2005) and southeastern Sicily (rarely; Caruso and Cosentino, 2014). The ecomorphotype A. cf. A. lessonii is found in 2-42m water depth around Linosa (4.4-25%) and A. cf. A. papillosa is distributed in 8-11m water depth around Linosa and Lampedusa (0.9-10%), (Caruso and Cosentino, 2014). Amphistegina lobifera shows especially high frequencies in the center of invasion (Israel and Turkey), although it may also occur in high frequencies along the range expansion front (up tp 97% around the Pelagian Islands/Caruso and Cosentino, 2014 and >50%

around Greece/Aegean Sea/Triantaphyllou et al. 2005). Living A. lobifera individuals may reach a density of 230.000-310.000 individuals/m² on rocky substrate and 3.75g/5g sediment around Turkey, indicating a deposition rate of 2-4.5cm/year (Meric et al. 2008a; Yokes and Meric, 2009; Fig. 7B-D).

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Along the coast of Turkey, invasions of amphisteginids resulted in sedimentary layers of 60-80 cm of pure amphisteginid, carbonate creating an immense ecological problem by changing the whole habitat structure and altering species composition of the coastal ecosystem (Meric et al. 2008a; Yokes and Meric, 2009). Waves carry amphisteginid tests to the shores, where they accumulate in small bays, thus changing gravelly shores to sandy beaches, with profound implications for native biotas and ecosystems (Yokes and Meric, 2009). Along the Israel rocky coast, Amphistegina lobifera is by far the most common species in shelf areas, taking over the local foraminiferal assemblage by occurring throughout the year, with a frequency of 180 individuals/g sediment (Hyams et al. 2002) and a contribution of 200g CaCO3m²yr^-1 (Gruber et al. 2007). In the Aegean Sea, it is the dominant foraminiferal species in southern and central regions, sometimes exceeding 50% of the assemblages (Triantaphyllou et al. 2009; Koukouisoura et al. 2010, 2011). As a result of the massive deposition of tests, A. lobifera is altering habitats and shorelines along the eastern Mediterranean Sea by the deposition of large amounts of sand-sized (0.5-2mm) soft substrates (Yokes and Meric, 2009;

Streftaris and Zenetos, 2006; Hyams et al. 2002, 2008). The average Mediterranean carbonate production by corals and other bioconstructors has been reported to be approximately 1 kg of CaCO3

per m² per year (Bianchi, 2007). Amphistegina spp. is therefore currently contributing a significant portion of the local carbonate budget, and due to its abundance, ubiquity and appearance in monocultures can be considered true ecosystem engineers (Langer et al. 2012; Weinmann et al. 2013b, Thissen and Langer, 2017) in the sense of Jones et al. (1994, 1997).

According to Langer and Hottinger (2000) amphisteginid foraminifera are delimited by the 14°C winter isotherm, and laboratory experiments showed that Amphistegina only ceased all movement below 12°C (Zmiri et al. 1974). It’s presence in the northern Aegean Sea and in the eastern Sea of Marmara, however, indicates an adaptation to lower water temperatures (Yokes and Meric, 2009 Triantaphyllou et al. 2012). The upper temperature limits of amphisteginid foraminifera are currently not known but vital populations thriving in tidal pools of eastern Africa and Raja Ampat indicate temperatures far beyond 30 °C (Langer unpubl. data; Weinmann et al. 2013b).

Since the reintroduction of Amphistegina spp. in the Mediterranean Sea to the eastern Mediterranean,

~ 140 years ago, it has crossed a total distance of approximately 1750km suggesting a dispersal rate of 12.5km/year (Langer et al. 2012; Weinmann et al. 2013b). Applied species distribution modeling for this taxon suggests a potential latitudinal expansion of Amphistegina spp. ranging between 515km in 2050 and 525 km in 2100, so that they are expected to migrate into the Adriatic Sea by the year 2050 and migrate west of Corsica and Sardinia by the year 2100 with an average dispersal rate of ~ 13.82km and ~ 11.76km per year respectively (Fig. 8; Weinmann et al. 2013b). Environmental factors such as calcite, nitrate and minimum and maximum temperature are the most important predictors for the model (Weinmann et al. 2013b).

The establishment and proliferating of foraminifera with a tendency to build monocultures may affect rates of carbonate production and may negatively impact the relationship between biodiversity and ecosystem functioning, resulting in biotic communities that are functionally more susceptible to environmental stress (Wallentius and Nyberg, 2007; Weinmann et al. 2013b). Although most of the introduced foraminifera are integrated in small proportions within native foraminiferal assemblages, some migrants have locally become dominant. Invasive species rapidly adapt to new environments, acting as consumers, prey, competitors, or disturbers, and provide evidence for biotic homogenization of foraminiferal faunal assemblages due to human-mediated breaching of biogeographic barriers (Calvo-Marclese and Langer, 2010). Therefore, their impact requires monitoring and detailed consideration, as newly established tropical benthic foraminifera will define a new Mediterranean geological phase for the future paleoecologists (Por, 2009).

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Fig. 8 (A) Species Distribution Models (SDM’s) for Amphistegina spp. under current and future climates as projected by Maxent (modified after Weinmann et al. 2013b). Probability of presence is indicated by habitat suitability values ranging from high (1, red areas) to very low (0.1813, light blue areas). Black stars indicate currently known distribution limits of Amphistegina spp. in Tunisia, Malta, Corfu and the northern Aegean Sea.

Gray hatched areas indicate areas of possible extrapolation of the model due to predictor values being outside the training range (MESS). (B) Species Distribution Model under climate conditions projected for 2050. Note the ongoing range expansion into the western Mediterranean. Habitat suitability is increasing around Italy. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of Weinmann et al. 2013b).