Climate-Driven Range Extension of Amphistegina (Protista,Foraminiferida): Models of Current and Predicted Future Ranges

Species-range expansions are a predicted and realized consequence of global climate change. Climate warming and the poleward widening of the tropical belt have induced range shifts in a variety of marine and terrestrial species. Range expansions may have broad implications on native biota and ecosystem functioning as shifting species may perturb recipient communities. Larger symbiont-bearing foraminifera constitute ubiquitous and prominent components of shallow water ecosystems, and range shifts of these important protists are likely to trigger changes in ecosystem functioning. We have used historical and newly acquired occurrence records to compute current range shifts of Amphistegina spp., a larger symbiont-bearing foraminifera, along the eastern coastline of Africa and compare them to analogous range shifts currently observed in the Mediterranean Sea. The study provides new evidence that amphisteginid foraminifera are rapidly progressing southwestward, closely approaching Port Edward (South Africa) at 31°S. To project future species distributions, we applied a species distribution model (SDM) based on ecological niche constraints of current distribution ranges. Our model indicates that further warming is likely to cause a continued range extension, and predicts dispersal along nearly the entire southeastern coast of Africa. The average rates of amphisteginid range shift were computed between 8 and 2.7 km year⁻¹, and are projected to lead to a total southward range expansion of 267 km, or 2.4° latitude, in the year 2100. Our results corroborate findings from the fossil record that some larger symbiont-bearing foraminifera cope well with rising water temperatures and are beneficiaries of global climate change.     

The tropical history and future of the Mediterranean biota and the West African enigma

Aim Since the opening of the Suez Canal in 1869, many tropical taxa from the Indo‐West Pacific (IWP) realm have entered the Mediterranean Sea, which is experiencing rising temperatures. My aims are: (1) to compare biogeographically this tropical transformation of the Mediterranean biota with the tropical faunas of the Mediterranean and adjacent southern European and West African seas during the Late Oligocene to Pliocene interval; (2) to infer the relative contributions of the tropical eastern Atlantic and IWP to the tropical component of the marine biota in southern Europe; and (3) to understand why West Africa is not now a major source of warm‐water species. Location Southern Europe, including the Mediterranean Sea, and the coast of tropical West Africa. Methods I surveyed the literature on fossil and living shell‐bearing molluscs to infer the sources and fates of tropical subgenus‐level taxa living in southern Europe and West Africa during the Late Oligocene to Pliocene interval. Results Ninety‐four taxa disappeared from the tropical eastern Atlantic (including the Mediterranean) but persisted elsewhere in the tropics, mainly in the IWP (81 taxa, 86%) and to a lesser extent in tropical America (36 taxa, 38%). Nine taxa inferred to have arrived in the tropical eastern Atlantic from the west after the Pliocene did not enter the Mediterranean. The modern West African fauna is today isolated from that of other parts of the marine tropics. Main conclusions Taxa now entering the Mediterranean through the Suez Canal are re‐establishing a link with the IWP that last existed 16 million years ago. This IWP element, which evolved under oligotrophic conditions and under a regime of intense anti‐predatory selection, will continue to expand in the increasingly warm and increasingly oligotrophic Mediterranean. The IWP source fauna contrasts with the tropical West African biota, which evolved under productive conditions and in a regime of less anti‐predatory specialization. Until now, the post‐Pliocene West African source area has been isolated from the Mediterranean by cold upwelling. If further warming should reduce this barrier, as occurred during the productive and warm Early Pliocene, the Mediterranean could become a meeting place for two tropical faunas of contrasting source conditions.     

Recent Invasion of the Symbiont-Bearing Foraminifera Pararotalia into the Eastern Mediterranean Facilitated by the Ongoing Warming Trend

The eastern Mediterranean is a hotspot of biological invasions. Numerous species of Indo-pacific origin have colonized the Mediterranean in recent times, including tropical symbiont-bearing foraminifera. Among these is the species Pararotalia calcariformata. Unlike other invasive foraminifera, this species was discovered only two decades ago and is restricted to the eastern Mediterranean coast. Combining ecological, genetic and physiological observations, we attempt to explain the recent invasion of this species in the Mediterranean Sea. Using morphological and genetic data, we confirm the species attribution to P. calcariformata McCulloch 1977 and identify its symbionts as a consortium of diatom species dominated by Minutocellus polymorphus. We document photosynthetic activity of its endosymbionts using Pulse Amplitude Modulated Fluorometry and test the effects of elevated temperatures on growth rates of asexual offspring. The culturing of asexual offspring for 120 days shows a 30-day period of rapid growth followed by a period of slower growth. A subsequent 48-day temperature sensitivity experiment indicates a similar developmental pathway and high growth rate at 28°C, whereas an almost complete inhibition of growth was observed at 20°C and 35°C. This indicates that the offspring of this species may have lower tolerance to cold temperatures than what would be expected for species native to the Mediterranean. We expand this hypothesis by applying a Species Distribution Model (SDM) based on modern occurrences in the Mediterranean using three environmental variables: irradiance, turbidity and yearly minimum temperature. The model reproduces the observed restricted distribution and indicates that the range of the species will drastically expand westwards under future global change scenarios. We conclude that P. calcariformata established a population in the Levant because of the recent warming in the region. In line with observations from other groups of organisms, our results indicate that continued warming of the eastern Mediterranean will facilitate the invasion of more tropical marine taxa into the Mediterranean, disturbing local biodiversity and ecosystem structure.     

Foraminiferal response to the Northeast Monsoon in the western and southern Arabian Sea

Sediments from the western and southern part of the Arabian Sea were collected periodically in the spring intermonsoon between March and May 1997 and additionally at the end of the Northeast Monsoon in February 1998. Assemblages of Rose Bengal stained, living deep-sea benthic foraminifera, their densities, vertical distribution pattern, and diversity were analysed after the Northeast Monsoon and short-time changes were recorded. In the western Arabian Sea, foraminiferal numbers increased steadily between March and the beginning of May, especially in the smaller size classes (30–63 μm, 63–125 μm). At the same time, the deepening of the foraminiferal living horizon, variable diversity and rapid variations between dominant foraminiferal communities were observed. We interpret these observations as the time-dependent response of benthic foraminifera to enhanced organic carbon fluxes during and after the Northeast Monsoon. In the southern Arabian Sea, constant low foraminiferal abundances during time, no distinctive change in the vertical distribution, reduced diversity, and more stable foraminiferal communities were noticed, which indicates no or little influence of the Northeast Monsoon to benthic foraminifera in this region.     

The Biodiversity of the Mediterranean Sea: Estimates,Patterns, and Threats

The Mediterranean Sea is a marine biodiversity hot spot. Here we combined an extensive literature analysis with expert opinions to update publicly available estimates of major taxa in this marine ecosystem and to revise and update several species lists. We also assessed overall spatial and temporal patterns of species diversity and identified major changes and threats. Our results listed approximately 17,000 marine species occurring in the Mediterranean Sea. However, our estimates of marine diversity are still incomplete as yet—undescribed species will be added in the future. Diversity for microbes is substantially underestimated, and the deep-sea areas and portions of the southern and eastern region are still poorly known. In addition, the invasion of alien species is a crucial factor that will continue to change the biodiversity of the Mediterranean, mainly in its eastern basin that can spread rapidly northwards and westwards due to the warming of the Mediterranean Sea. Spatial patterns showed a general decrease in biodiversity from northwestern to southeastern regions following a gradient of production, with some exceptions and caution due to gaps in our knowledge of the biota along the southern and eastern rims. Biodiversity was also generally higher in coastal areas and continental shelves, and decreases with depth. Temporal trends indicated that overexploitation and habitat loss have been the main human drivers of historical changes in biodiversity. At present, habitat loss and degradation, followed by fishing impacts, pollution, climate change, eutrophication, and the establishment of alien species are the most important threats and affect the greatest number of taxonomic groups. All these impacts are expected to grow in importance in the future, especially climate change and habitat degradation. The spatial identification of hot spots highlighted the ecological importance of most of the western Mediterranean shelves (and in particular, the Strait of Gibraltar and the adjacent Alboran Sea), western African coast, the Adriatic, and the Aegean Sea, which show high concentrations of endangered, threatened, or vulnerable species. The Levantine Basin, severely impacted by the invasion of species, is endangered as well.This abstract has been translated to other languages (File S1).     

Distribution and morphology of the sea lamprey from the Balkan coast of the Adriatic Sea

In contrast to the Apennine Peninsula coast, the relatively rare occurrence of sea lampreys Petromyzon marinus in the Balkan Peninsula (eastern coast of the Adriatic Sea) is probably due to the closeness of the steep mountains causing unsuitable hydrological conditions of streams and impeded access to the coast. Most specimens are probably represented by invaders carried from the Mediterranean and other regions of the Adriatic Sea. Morphology was similar to that recorded for the sea lampreys from other geographical regions.     

Isolated population of the Middle Eastern Phoenicolacerta laevis from the Georgian Black Sea Coast,and its genetic closeness to populations from southern Turkey

The Lebanon Lizard (Phoenicolacerta laevis) occurs on the Levantine coast and scattered populations are found in isolated coastal habitats along the southern and south-western coast of Turkey. We found an isolated but dense population of this species at and around the castle of Anaklia on Georgia’s Black Sea Coast, near the mouth of the river Enguri. The analysis of mitochondrial cytochrome b sequence suggests closeness of this population to the populations in the provinces of Kahramanmara?, Adana and Içel in southern Turkey, rather than to those in Lebanon and Israel. It is thought that the species was introduced from a Turkish region to Anaklia, which was an important trade location at the eastern Black Sea coast until the late 18^th century. This is the first established location of this species outside the eastern Mediterranean area. Climate and competition with rock lizards of the genus Darevskia are the most likely reasons preventing expansion of the species into the neighboring areas of Western Georgia.     

The impact of seawater temperature on coral growth parameters of the colonial coral Cladocora caespitosa (Anthozoa, Scleractinia) in the eastern Adriatic Sea

The scleractinian coral Cladocora caespitosa deserves a special place among the major carbonate bioconstructors of the Mediterranean Sea. Annual coral skeleton growth, coral calcification, and skeleton density of the colonial coral C. caespitosa taken from 25 locations in the eastern Adriatic Sea were analyzed and compared with annual sea surface temperatures (SST). The growth rates of the coral C. caespitosa from the 25 stations in the Adriatic Sea ranged from 1.92 to 4.19?mm per year, with higher growth rates of the investigated corallites in the southern part of the Adriatic Sea. These growth rates are similar to those measured in other areas of the Mediterranean Sea. The correlation between coral growth and sea temperatures in the Adriatic Sea is seen as follows: An X-radiograph analysis of coral growth in C. caespitosa colonies that are over 60?years old showed that higher growth rates of this coral coincided with a warmer period in the Mediterranean Sea. A positive significant correlation exists between corallite growth rates and SST and coral calcification and SST. A negative correlation exists between coral density and SST. Coral growth rates also showed a correlation with higher eutrophication caused by nearby fish farms, along with a greater depth of the investigated colonies and high bottom currents.     

Patterns of diversity of the north-eastern Atlantic blenniid fish fauna (Pisces: Blenniidae)

This paper presents an analysis of the distributional patterns of blenniids (Pisces: Blenniidae) in the north‐eastern Atlantic. Two peaks of species diversity were found, both in terms of number of species and number of endemics: one in the tropical African coast and another in the Mediterranean Sea. A cluster analysis of similarity values (Jaccard coefficient) among the eastern Atlantic zoogeographical areas, revealed the following groups: a north temperate group, a tropical group formed by the tropical African coast and Mauritania, another group formed by the islands of Cape Verde, a south temperate group (South Africa), and a southern Atlantic group formed by the islands of Ascension and St Helena. Within the north temperate group, the subgroups with higher similarities were: Azores and Madeira, Canary Islands and Morocco, and the Mediterranean and the Atlantic coast of the Iberian Peninsula. Based on affinity indices, the probable directions of faunal flows were inferred. The tropical coast of Africa and the Mediterranean emerged from this analysis as probable speciation centres of the north‐eastern Atlantic blenniid fauna. The Mediterranean may have also acted as a refuge during glacial periods.     

Foraminifera in a New Zealand salt marsh and their suitability as sea-level indicators

Vertical distributions of live and dead foraminiferal abundances are investigated in a salt marsh at Pounawea in southeastern New Zealand for potential use in Holocene sea-level reconstructions. Statistical analyses are conducted to determine whether dead foraminiferal abundances can be utilised as a proxy for elevation in southeastern New Zealand. It is concluded that dead salt-marsh foraminifera, which can predict elevations to within ± 5 cm or better, are precise sea-level proxies. Holocene sea-level reconstructions along the tectonically stable Catlins Coast based on fossil salt-marsh foraminifera can therefore serve as a potential baseline tool to estimate relative vertical tectonic displacement along tectonically active coasts in New Zealand.     

Tracing the introduction history of the invasive swimming crab <Emphasis Type="Italic">Charybdis hellerii</Emphasis> (A. Milne-Edwards, 1867) in the Western Atlantic: evidences of high genetic diversity and multiple introductions

The swimming crab Charybdis hellerii is an invader with global distribution in warm waters. Native to the Indo-Pacific, this species invaded the eastern Mediterranean Sea after the Suez Canal opening. In 1987, it was first reported in the Western Atlantic, probably transported via ballast water of ships. Since then, it has been registered from many localities along the American coast from the USA to southern Brazil where it has rapidly established reproducing populations. Our main aim was to investigate the introduction history of this species along the American coast, using a phylogeographic approach. Additionally, we attempted to clarify the identity of this invasive species by molecular analyses and morphological assessment in order to provide a basis for our main investigation. C. hellerii was confirmed as a single species, but both cytochrome c oxidase subunit I and 16S rDNA revealed a genetic structure, splitting the potential source populations of American introductions into two groups: “western Indian Ocean and Mediterranean Sea” (WIO + MS) versus “eastern Indian + western Pacific oceans” (EIO + WPO). Most specimens from America clustered with the former group, supporting the hypothesis that the Mediterranean Sea represented the main source of Western Atlantic populations. However, the clustering of animals from southern Brazil with the latter group indicates that introductions from the eastern Indian or Pacific oceans must also have occurred. The existence of a third group, found exclusively within the American range and genetically related to EIO + WPO, also indicates an independent introduction from an unsampled locality from the native range. The haplotype and nucleotide diversities of American localities were comparable to those of source populations, contradicting a founder effect prediction. This finding might be related to the high propagule pressure associated with introductions via ballast water and the occurrence of multiple introductions from genetic distinct sources. The direct comparison of the haplotype numbers suggested no genetic bottleneck during introduction from the Mediterranean Sea, but a bottleneck might have occurred during introductions from the eastern Indian or Pacific oceans.     

Molecular Phylogeny and Ecology of Textularia agglutinans d’Orbigny from the Mediterranean Coast of Israel: A Case of a Successful New Incumbent

Textularia agglutinans d’Orbigny is a non-symbiont bearing and comparatively large benthic foraminiferal species with a widespread distribution across all oceans. In recent years, its populations have considerably expanded along the Israeli Mediterranean coast of the eastern Levantine basin. Despite its exceptionally widespread occurrence, no molecular data have yet been obtained. This study provides the first ribosomal DNA sequences of T. agglutinans complemented with morphological and ecological characterization, which are based on material collected during environmental monitoring of the hard bottom habitats along the Israeli Mediterranean coast, and from the Gulf of Elat (northern Red Sea). Our phylogenetic analyses reveal that all specimens from both provinces belong to the same genetic population, regardless their morphological variability. These results indicate that modern population of T. agglutinans found on the Mediterranean coast of Israel is probably Lessepsian. Our study also reveals that T. agglutinans has an epiphytic life mode, which probably enabled its successful colonization of the hard bottom habitats, at the Mediterranean coast of Israel, which consist of a diverse community of macroalgae. Our study further indicates that the species does not tolerate high SST (> 35°C), which will probably prevent its future expansion in the easternmost Mediterranean in light of the expected rise in temperatures.     

Paranthias furcifer (Perciformes: Serranidae), a new alien fish in the Mediterranean Sea

A specimen of a creole fish Paranthias furcifer (285 mm total length) was captured in Marina Bay (Croatian coast) in the eastern Adriatic Sea. This is the first Mediterranean record of this species. The possible modes of introduction of species are discussed.     

Fistularia commersonii in the Mediterranean Sea: invasion history and distribution modeling based on presence-only records

The bluespotted cornetfish (Fistularia commersonii) (Osteichtyes, Fistulariidae) is considered to be one of the most invasive species of the Mediterranean Sea and Europe but only scattered information exists on its distribution and abundance. Here we collated the available species records, following its first detection in the Mediterranean Sea, in January 2000, until October 2011. A total of 191 observations were used to reconstruct the invasion sequence, to provide estimates of the rate of spread and to construct an environmental suitability model based on six biophysical variables and the maximum entropy approach. The results showed that colonization of the Mediterranean Sea proceeded in parallel along the southern and northern rim of the Basin at speeds that reached 1,000–1,500 km year^?1 with a clear decrease in the rate of spread at the Sicily Strait. The most important explanatory variables for describing the distribution of F. commersonii were mean depth (explaining 32.4 % of the data variance), chlorophyll-a (29.3 %), and salinity (18.4 %). Coastal areas with relatively low chlorophyll-a concentrations and high salinity were the preferred habitat of the bluespotted cornetfish in its invaded range. Conversely, extreme productivity (highly eutrophic or highly oligotrophic), low salinity and cold temperatures provided abiotic resistance to this invasion. Areas of high environmental suitability were identified along the northern coasts of the Levantine Sea, Dodecanese, Sicily Strait and Tyrrhenian Sea. In contrast, the north Aegean Sea, the Adriatic and the Alboran Sea, the Nile Delta, the western coasts of Egypt and Cyrenaica were unfavourable for the invasion. Despite some limits due to the model’s resolution scale, these general predictions provide new insights into the F. commersonii invasion, indicating abiotic factors of primary importance in shaping the distribution of this species in its invaded range.     

Red to Mediterranean Sea bioinvasion: natural drift through the Suez Canal,or anthropogenic transport?

The biota of the eastern basin of the Mediterranean Sea has experienced dramatic changes in the last decades, in part as a result of the massive invasion of Red Sea species. The mechanism generally hypothesized for the 'Red-to-Med' invasion is that of natural dispersal through the Suez Canal. To date, however, this hypothesis has not been tested. This study examines the mode of invasion, using as a model the mussel Brachidontes pharaonis, an acclaimed 'Lessepsian migrant' that thrives along the eastern Mediterranean coast. Our findings reveal two distinct lineages of haplotypes, and five possible explanations are discussed for this observation. We show that the genetic exchange among the Mediterranean, Gulf of Suez and the northern Red Sea is sufficiently large to counteract the build up of sequential genetic structure. Nevertheless, these basins are rich in unique haplotypes of unknown origin. We propose that it is historic secondary contact, an ongoing anthropogenic transport or both processes, that participate in driving the population dynamics of B. pharaonis in the Mediterranean and northern Red Sea.     

Linnaeus' Neptunea (Mollusca: Gastropoda)

Three species of the arcto-boreal, large gastropod Neptunea , described by Linnaeus in 1758 and 1771, occur in large numbers over wide areas of the inshore North Atlantic and adjacent Arctic seas and are conspicuous among Pliocene and Pleistocene molluscs in the Icelandic, North Sea, and western Mediterranean basins. Selections of lectotypes for these species from shells in the collection of the Linnean Society of London, and designations of their type localities, establish the identity of Linnaeus' neptunes and more accurately determine their geographic and geologic distribution. The geographic range of Neptunea (Neptunea) antiqua (L.), the type species, now extends from southern Norway to the northern Biscay coast of France and from the westernmost Baltic Sea to southwestern Ireland; this species also occurs in Pliocene-Holocene marine deposits in West and East Germany, Sweden, the Netherlands, England and France. Its type locality is determined to be the North Sea. N. (Neptunea) despecta (L.) lives in the eastern Canadian Arctic, off southern Greenland, the Barents Sea, and North Atlantic as far south as Massachusetts and Portugal; it also occurs in Pliocene-Holocene strata of eastern Canada, east-central Greenland, Norway (including Svalbard), the Soviet Union, Sweden and England. Its type locality is determined to be the postglacial deposits at Uddevalla in southwestern Sweden. N. (Sulcosipho) contraria (L.) now extends from the southern Biscay coast of France to Cape Spartel, Morocco; this species also occurs in Pleistocene and lower Holocene sequences of the western Mediterranean. Its type locality is determined to be Vigo Bay, Spain. A closely related fossil species, N. (S.) angulata (S. V. Wood), occurs in Pliocene and Pleistocene deposits of the North Sea basin.     

Mangrove expansion and salt marsh decline at mangrove poleward limits

Mangroves are species of halophytic intertidal trees and shrubs derived from tropical genera and are likely delimited in latitudinal range by varying sensitivity to cold. There is now sufficient evidence that mangrove species have proliferated at or near their poleward limits on at least five continents over the past half century, at the expense of salt marsh. Avicennia is the most cold‐tolerant genus worldwide, and is the subject of most of the observed changes. Avicennia germinans has extended in range along the USA Atlantic coast and expanded into salt marsh as a consequence of lower frost frequency and intensity in the southern USA. The genus has also expanded into salt marsh at its southern limit in Peru, and on the Pacific coast of Mexico. Mangroves of several species have expanded in extent and replaced salt marsh where protected within mangrove reserves in Guangdong Province, China. In south‐eastern Australia, the expansion of Avicennia marina into salt marshes is now well documented, and Rhizophora stylosa has extended its range southward, while showing strong population growth within estuaries along its southern limits in northern New South Wales. Avicennia marina has extended its range southwards in South Africa. The changes are consistent with the poleward extension of temperature thresholds coincident with sea‐level rise, although the specific mechanism of range extension might be complicated by limitations on dispersal or other factors. The shift from salt marsh to mangrove dominance on subtropical and temperate shorelines has important implications for ecological structure, function, and global change adaptation.     

Phylogeographic evidence for the postglacial colonization of the North and Baltic Sea coasts from inland glacial refugia by Triglochin maritima L.

We investigated the geographical distribution of genetic variation in 67 individuals of Triglochin maritima from 38 localities across Europe using AFLP markers. Analysis of genetic variation resulted in the recognition of two major genetic groups. Apart from few geographical outliers, these are distributed (1) along the Atlantic coasts of Portugal, Spain and France and (2) in the North Sea area, the Baltic Sea area, at central European inland localities, the northern Adriatic Sea coast and the Mediterranean coast of southwest France. Considering possible range shifts of T. maritima in reaction to Quaternary climatic changes as deduced from the present-day northern temperature limit of the species, Quaternary changes of coastline in the North Sea area and the very recent origin of the Baltic Sea, we conclude that the coastal populations of T. maritima in the North Sea and Baltic Sea areas originated from inland populations.     

Alien species in the Mediterranean Sea—which, when, where, why?

A critical evaluation of more than 2,200 publications, some dating back to the late 1800s, established the presence, and traced the spatio-temporal spread, of 558 alien metazoan species in the Mediterranean Sea. The majority of aliens in the eastern Mediterranean entered through the Suez Canal, whereas mariculture and shipping are powerful means of introduction in the northwestern Mediterranean and in the Adriatic Sea. Most aliens are thermophilic species. The possible causes for the epic scale of invasion in the Mediterranean Sea are discussed. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users. Guest editors: J. Davenport, G. Burnell, T. Cross, M. Emmerson, R. McAllen, R. Ramsay & E. Rogan Challenges to Marine Ecosystems