The genetic diversity of planktic foraminifera and the global distribution of ribosomal RNA genotypes

Fossil planktic foraminifers in the ocean sediments play an unparalleled role in our understanding of the oceanographic environment in the past. An in depth knowledge of their diversity, ecology and biogeography in the modern ocean lies central to the interpretation of the fossil assemblages. In comparison with their benthic counterparts, planktic foraminifera have a very limited diversity of around fifty extant morphospecies. Their morphospecies diversity peaks in the sub-tropics and decreases steeply towards the poles. Traditional species concepts have partitioned morphological types into distinct species (morphospecies) based on test shape, but genetic studies show that individual morphospecies are actually complexes of several discrete genetic types (genotypes). Many of these genotypes have distinct ecologies and novel adaptations that are consistent with species-level classification, indicating that the true diversity of planktic foraminifers has been greatly underestimated. Although planktic foraminifera are clearly capable of long-distance dispersal, they may be constrained by both physical and ecological barriers that vary according to the evolutionary history and ecology of the individual genotypes within a morphospecies. These differences lead to diverse biogeographies. Here, we provide an overview of the genetic and biogeographic data available to date for the planktic foraminifera and present global biogeographies highlighting the distribution of genetic types in the eight planktic foraminiferal morphospecies for which detailed molecular evidence is available.     

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.     

Benthic foraminiferal fauna during the time of the Indian-Asian contact, in southern Balochistan, Pakistan

Cretaceous and early Paleocene benthic foraminifera were studied from one section along the western Gaj River, southern Balochistan, Pakistan, to reconstruct the paleoenvironment of the Tethys Sea during the Indian-Asian contact. We recognize three lithostratigraphic units in ascending order: the Mughal Kot Formation, the Pab Sandstone, and the Jamburo Group. Both the Maastrichtian Mughal Kot Formation, which consists of shale with grey marly limestone, and the Maastrichtian Pab Sandstone, which consists of quartzose sandstone, indicate an open ocean environment as they have diversified planktic and benthic foraminiferal assemblages. The Maastrichtian-Paleocene Jamburo Group, consisting of dark grey, calcareous shale and marlstone with some sulfide grains, is characterized by low diversities of benthic assemblages. The change to the lower diversities may be associated with the development of poor circulation of deeper water that was caused by narrowing of the Tethys Sea.The Trochammina spp. Assemblage from the Jamburo Group, which can be correlated with flysch-type agglutinated foraminiferal assemblages, has a low benthic species diversity, indicating an unfavorable condition for calcareous foraminifera because of the development of oxygen-depleted water. The absolute abundance of agglutinated specimens shows a remarkable change from low numbers in the Maastrichtian to high ones in the Paleocene. The benthic foraminiferal evidence supports the hypothesis that the collision of the Asian and Indian plates occurred near the end of the Cretaceous.     

Metabarcoding reveals high diversity of benthic foraminifera linked to water masses circulation at coastal Svalbard

Arctic marine biodiversity is undergoing rapid changes due to global warming and modifications of oceanic water masses circulation. These changes have been demonstrated in the case of mega- and macrofauna, but much less is known about their impact on the biodiversity of smaller size organisms, such as foraminifera that represent a main component of meiofauna in the Arctic. Several studies analyzed the distribution and diversity of Arctic foraminifera. However, all these studies are based exclusively on the morphological identification of specimens sorted from sediment samples. Here, we present the first assessment of Arctic foraminifera diversity based on metabarcoding of sediment DNA samples collected in fjords and open sea areas in the Svalbard Archipelago. We obtained a total of 5,968,786 reads that represented 1384 amplicon sequence variants (ASVs). More than half of the ASVs (51.7%) could not be assigned to any group in the reference database suggesting a high genetic novelty of Svalbard foraminifera. The sieved and unsieved samples resolved comparable communities, sharing 1023 ASVs, comprising over 97% of reads. Our analyses show that the foraminiferal assemblage differs between the localities, with communities distinctly separated between fjord and open sea stations. Each locality was characterized by a specific assemblage, with only a small overlap in the case of open sea areas. Our study demonstrates a clear pattern of the influence of water masses on the structure of foraminiferal communities. The stations situated on the western coast of Svalbard that are strongly influenced by warm and salty Atlantic water (AW) are characterized by much higher diversity than stations in the northern and eastern part, where the impact of AW is less pronounced. This high diversity and specificity of Svalbard foraminifera associated with water mass distribution indicate that the foraminiferal metabarcoding data can be very useful for inferring present and past environmental conditions in the Arctic.     

Deep-sea benthic foraminiferal recolonization of the 1991 Mt. Pinatubo ash layer in the South China Sea

A census count of Rose Bengal stained benthic foraminifera from the surface area on top of a 2 to 6 cm thick ashfall layer at three deep water stations along the western margin of the Philippines exhibits a unique assemblage composition of benthic foraminifera. The total number of benthic foraminifera is low and the ratio of living individuals to empty tests is high. Specific diversity is low, with a significant dominance of infaunal morphotypes including species of the genus Reophax (R. scorpiurus, R. bilocularis and R. dentaliniformis), which are regarded as successful recolonizers. Assemblages below the ash layers are diverse and contain many epifaunal suspension-feeding agglutinated and calcareous foraminifera. The 1991 Mt. Pinatubo eruption caused mass mortality of benthic foraminifera in a vast area of the eastern South China Sea followed by step-wise recolonization of the ash substrate. Three years after the eruption, the benthic foraminiferal community structure is still far from recovery to background levels.     

Environmental monitoring through protist next‐generation sequencing metabarcoding: assessing the impact of fish farming on benthic foraminifera communities

The measurement of species diversity represents a powerful tool for assessing the impacts of human activities on marine ecosystems. Traditionally, the impact of fish farming on the coastal environment is evaluated by monitoring the dynamics of macrobenthic infaunal populations. However, taxonomic sorting and morphology‐based identification of the macrobenthos demand highly trained specialists and are extremely time‐consuming and costly, making it unsuitable for large‐scale biomonitoring efforts involving numerous samples. Here, we propose to alleviate this laborious task by developing protist metabarcoding tools based on next‐generation sequencing (NGS) of environmental DNA and RNA extracted from sediment samples. In this study, we analysed the response of benthic foraminiferal communities to the variation of environmental gradients associated with salmon farms in Scotland. We investigated the foraminiferal diversity based on ribosomal minibarcode sequences generated by the Illumina NGS technology. We compared the molecular data with morphospecies counts and with environmental gradients, including distance to cages and redox used as a proxy for sediment oxygenation. Our study revealed high variations between foraminiferal communities collected in the vicinity of fish farms and at distant locations. We found evidence for species richness decrease in impacted sites, especially visible in the RNA data. We also detected some candidate bioindicator foraminiferal species. Based on this proof‐of‐concept study, we conclude that NGS metabarcoding using foraminifera and other protists has potential to become a new tool for surveying the impact of aquaculture and other industrial activities in the marine environment.     

Bipolar gene flow in deep-sea benthic foraminifera

Despite its often featureless appearance, the deep-ocean floor includes some of the most diverse habitats on Earth. However, the accurate assessment of global deep-sea diversity is impeded by a paucity of data on the geographical ranges of bottom-dwelling species, particularly at the genetic level. Here, we present molecular evidence for exceptionally wide distribution of benthic foraminifera, which constitute the major part of deep-sea meiofauna. Our analyses of nuclear ribosomal RNA genes revealed high genetic similarity between Arctic and Antarctic populations of three common deep-sea foraminiferal species (Epistominella exigua, Cibicides wuellerstorfi and Oridorsalis umbonatus), separated by distances of up to 17, 000 km. Our results contrast with the substantial level of cryptic diversity usually revealed by molecular studies, of shallow-water benthic and planktonic marine organisms. The very broad ranges of the deep-sea foraminifera that we examined support the hypothesis of global distribution of small eukaryotes and suggest that deep-sea biodiversity may be more modest at global scales than present estimates suggest.     

Molecular Identification of Algal Endosymbionts in Large Miliolid Foraminifera: 1. Chlorophytes

Large miliolid foraminifers bear various types of algal endosymbionts including chlorophytes, dinoflagellates, rhodophytes, and diatoms. Symbiosis plays a key role in the adaptation of large foraminifera to survival and growth in oligotrophic seas. The identity and diversity of foraminiferal symbionts, however, remain largely unknown. In the present work we use ribosomal DNA (rDNA) sequences to identify chlorophyte endosymbionts in large miliolid foraminifera of the superfamily Soritacea. Partial 18S and complete Internal Transcribed Spacer (ITS) rDNA sequences were obtained from symbionts of eight species representing all genera of extant chlorophyte-bearing Soritacea. Phylogenetic analysis of the sequences confirms the previous fine structure-based identification of these endosymbionts as belonging to the genus Chlamydomonas. All foraminiferal symbionts form a monophyletic group closely related to Chlamydomonas noctigama. The group is composed of seven types identified in this study, including one previously morphologically described species, Chlamydomonas hedleyi. Each of these types can be considered as a separate species, based on the comparison of genetic differences observed between other established Chlamydomonas species. Several foraminiferal species share the same symbiont type, but only one species, Archaias angulatus, was found to bear more than one type.     

南海北部琼东南盆地BD-2井中新世有孔虫生物地层及沉积环境

南海北部琼东南盆地BD-2井中新世地层沉积连续,是琼东南盆地中新统较典型的钻井剖面之一。该井中新世地层中含丰富的有孔虫化石,共鉴定有孔虫62属98种,其中浮游有孔虫13属41种,底栖有孔虫49属57种。根据有孔虫标志种及螺旋浮游有孔虫旋向优势度的变化,对该井的有孔虫生物地层进行了详细划分,从早中新世至晚中新世共识别出11个有孔虫化石带或联合化石带。探讨了下中新统与中中新统,中中新统与上中新统界线的有孔虫划分标志。依据有孔虫丰度、分异度及组合特征,讨论了BD-2井从早中新世至晚中新世沉积环境演化特征。     

Phylogenetic incongruence between dinoflagellate endosymbionts (Symbiodinium) and their host foraminifera (Sorites): small-subunit ribosomal RNA gene sequence evidence

Phototrophic dinoflagellate zooxanthellae commonly occur as endosymbionts in many planktic and certain benthic foraminifera (soritids). Many taxonomic issues and specific identities of foraminiferal dinoflagellates are not yet resolved. To assess taxonomic affinities among other dinoflagellates, we have determined the complete nucleotide sequence of the small-subunit rRNA coding region from Symbiodinium sp., an endosymbiotic dinoflagellate of the larger foraminifer Sorites orbiculus. The poly merase chain reaction was adopted for the in vitro amplification of ribosomal DNA, utilizing primers complementary to conserved regions. PCR-amplified DNA was directly sequenced and the sequence was aligned to all complete 18S-rDNA dinoflagellate sequences currently available through GenBank. Apicomplexan, ciliate, chromistacean, and rhodophycean sequences were added to infer across-kingdom phylogenetic relationships. Phylogenetic analysis of aligned nucleotide sequences produced a single most parsimonious tree (generated by the branch and bound method of PAUP). The inferred phylogeny indicates that the dinoflagellate extracted from the foraminifer Sorites orbiculus is a sister taxon to the symbiont present in the larger foraminifera Marginopora kudakajimaensis, but only distantly related to the dinoflagellate isolated from the soritid Amphisorus hemprichii. The sequence heterogeneity demonstrates a high degree of genetic diversity among Symbiodinium-like zooxanthellae and re-emphasizes that they are a variety of distinct entities.The inferred molecular phylogenetic relationships among symbiotic dinoflagellates are not congruent with the foraminiferal phylogeny based on cladistic methodology. The lack of correlation between the evolutionary history of dinoflagellate symbionts and their foraminiferal hosts argues against co-evolution. This lack of co-evolution implies that flexible recombinations among hosts and symbionts are evolutionarily favorable over permanently associated lineages, at least in these benthic foraminifera.     

PFR2: a curated database of planktonic foraminifera 18S ribosomal DNA as a resource for studies of plankton ecology,biogeography and evolution

Planktonic foraminifera (Rhizaria) are ubiquitous marine pelagic protists producing calcareous shells with conspicuous morphology. They play an important role in the marine carbon cycle, and their exceptional fossil record serves as the basis for biochronostratigraphy and past climate reconstructions. A major worldwide sampling effort over the last two decades has resulted in the establishment of multiple large collections of cryopreserved individual planktonic foraminifera samples. Thousands of 18S rDNA partial sequences have been generated, representing all major known morphological taxa across their worldwide oceanic range. This comprehensive data coverage provides an opportunity to assess patterns of molecular ecology and evolution in a holistic way for an entire group of planktonic protists. We combined all available published and unpublished genetic data to build PFR², the Planktonic foraminifera Ribosomal Reference database. The first version of the database includes 3322 reference 18S rDNA sequences belonging to 32 of the 47 known morphospecies of extant planktonic foraminifera, collected from 460 oceanic stations. All sequences have been rigorously taxonomically curated using a six‐rank annotation system fully resolved to the morphological species level and linked to a series of metadata. The PFR² website, available at http://pfr2.sb-roscoff.fr , allows downloading the entire database or specific sections, as well as the identification of new planktonic foraminiferal sequences. Its novel, fully documented curation process integrates advances in morphological and molecular taxonomy. It allows for an increase in its taxonomic resolution and assures that integrity is maintained by including a complete contingency tracking of annotations and assuring that the annotations remain internally consistent.     

Planktic foraminifera from the mid-Cretaceous (Barremian–Early Albian) of the North Sea Basin: Palaeoecological and palaeoceanographic implications

A marine Cretaceous succession (Barremian–Albian) of a cored borehole (BGS 81/40), located in the Central North Sea Basin, has been examined with respect to its planktic and benthic foraminiferal content, as well as for calcareous nannofossils. The distribution patterns of foraminifera and calcareous nannofossils allow for a two fold division of the investigated interval. (1) The Barremian–earliest Aptian interval, which reflects a marine, temporary restricted setting. This is indicated by sporadic occurrences of planktic foraminifera with very rare planispiral forms suggesting short-term connections of the Boreal and Tethyan Realms. The benthic foraminiferal assemblages indicate aerobic, sometimes dysaerobic bottom-water conditions. High abundances of nannoconids in the Barremian suggest enhanced stratification and/or warm, oligotrophic surface water. (2) The late Aptian–early Albian interval, which was characterised by an open-oceanic environment with cool and aerobic surface water conditions. Planktic foraminifera are more abundant and diverse than in the lower interval. Trochospiral hedbergellids dominate the foraminiferal assemblages. The episodic occurrences of planispiral, clavate and trochospiral-flattened planktic morphotypes indicate the existence of a seaway between the Boreal and the Tethyan Realms. Aerobic to dysaerobic bottom-water conditions are suggested by the composition of the benthic foraminiferal assemblages. High abundances of cool-water taxa within the calcareous nannofossil assemblages indicate a cooling trend across the latest Aptian and earliest Albian.     

渤海莱州湾表层沉积物中底栖有孔虫分布特征及其环境意义

对渤海莱州湾海域240个站位表层沉积物中底栖有孔虫群落进行了分析,共鉴定常见的底栖有孔虫42种。结果表明,莱州湾表层沉积物中底栖有孔虫主要以玻璃质壳为主(平均丰度达70.9%),瓷质壳含量次之,胶结壳含量最低;玻璃质壳占有孔虫全群的百分含量,随水深的增加而增加;从黄河口向外海方向,有孔虫分异度和丰度都逐渐增大。该海域底栖有孔虫平面分布的主要控制因素为盐度和底质沉积物类型,大体可分为两个组合分区,I区为Ammonia beccarii-Quinqueloculina spp.组合,代表盐度较低的近岸海陆过渡浅水环境;II区为Cribrononionsub-incertum-Protelphidium tuberculatum组合,代表盐度较高的远岸内陆架环境。     

Environmental impacts on the benthic foraminiferal fauna in nearshore ecosystems

This review presents data on how natural and anthropogenic factors affect species composition, abundance, and test morphology of benthic foraminifera of the world oceans. Major emphasis is placed on high sensitivity of foraminifera to changes in the state of the environment, particularly in nearshore zones under anthropogenic impact. It is shown that benthic foraminifera can provide indicators of environmental conditions in marine ecosystems. The effects of mollusk and salmon aquaculture activities on the composition and distribution of foraminifera are considered. It is stressed that a distinction must be made between foraminiferal test morphology variations in response to natural and anthropogenic impacts.     

Benthic foraminiferal distributions in Chilean fjords: 47°S to 54°S

Surface sediment samples collected from the fjord region of southern Chile (47° to 54° South) were analyzed for benthic foraminifera. A total of 175 species were identified including agglutinated and calcareous benthic taxa. Hierarchical cluster analysis of the foraminiferal data resulted in the recognition of three distinct biofacies: inner-fjord, intermediate fjord and channel, and oceanic biofacies, geographically controlled by relative position between the Pacific Ocean and fjord heads. Similarity percentage (SIMPER) analysis identified key taxa in the definition of the biofacies that include Globocassidulina rossensis, Cassidulina laevigata and Bulimina notovata. Principal components analysis resulted in two principal components representing sediment size, and bottom water temperature and salinity.Regional distributions are strongly controlled by the oceanographic conditions influenced from the Pacific in the west and the glacial/freshwater input from the east. Localized distributions of foraminifera are controlled by conditions influenced by the physiography of the individual fjords and channels. The distribution of Chilean fjord foraminifera and their environmental associations are consistent with results from other temperate to high latitude fjord foraminiferal studies.     

Recent benthic foraminiferal assemblages from cold-water coral mounds in the Porcupine Seabight

Cold-water coral ecosystems are characterised by a high diversity and population density. Living and dead foraminiferal assemblages from 20 surface sediment samples from Galway and Propeller Mounds were analysed to describe the distribution patterns of benthic foraminifera on coral mounds in relation to different sedimentary facies. Hard substrates were examined to assess the foraminiferal microhabitats and diversities in the coral framework. We recognised 131 different species, of which 27 prefer an attached lifestyle. Epibenthic species are the main constituents of the living and dead foraminiferal assemblages. The frequent species Discanomalina coronata was associated with coral rubble, Cibicides refulgens showed preference to the off-mound sand veneer, and Uvigerina mediterranea displayed abundance maxima in the main depositional area on the southern flank of Galway Mound, and in the muds around Propeller Mound. The distribution of these species is rather governed by their specific ecological demands and microhabitat availability than by the sedimentary facies. Benthic foraminiferal assemblages from coral mounds fit well into basin-wide-scale distribution patterns of species along the western European continental margin. The diversity of the foraminiferal faunas is not higher on the carbonate mounds as in their vicinity. The living assemblages show a broad mid-slope diversity maximum between 500 and 1,300 m water depth, which is the depth interval of coral mound formation at the Celtic and Amorican Margin. The foraminiferal diversity maximum is about 700 m shallower than comparable maxima of nematodes and bivalves. This suggests that different processes are driving the foraminiferal and metazoan diversity patterns.     

Palaeoenvironmental conditions preceding the Messinian Salinity Crisis: A case study from Gavdos Island

The Messinian pre-evaporitic sedimentary succession of Gavdos Island (Metochia section) is a nearly uninterrupted succession of marine sediments, dominated by finely laminated diatomaceous marls, which are cyclically alternating with clayey diatomites and white diatomites. The qualitative and quantitative analysis of the planktonic foraminiferal fauna allowed the recognition of nine bioevents, which have been astronomically dated for the Mediterranean. The base of the diatomitic succession in Gavdos Island is dated at 6.722 Ma and the top at 6.015 Ma. The studied section contains benthic foraminiferal genera characteristic of an outer shelf to slope environment. The qualitative and quantitative analysis of this microfauna revealed three benthic foraminiferal fossil assemblages and the occurrence of allochthonous species transported into the bathyal environment by current activity. The cyclical pattern of the benthic foraminifera assemblages indicates that the studied sediments have been affected by repeated episodes of basin restriction characterized by low diversity benthic foraminifera populations, and a limited planktonic foraminifer association typified by shallow, surface-dwelling forms. This restriction was partly due to Antarctic cooling, which produced palaeo-Mediterranean sea-level oscillations during the Early Messinian, as a prelude to closure of the Atlantic connections. The relative impact of climatic versus tectonic control on sedimentation patterns within this basin is discussed.     

Molecular evidence for widespread occurrence of Foraminifera in soils

Environmental SSU rDNA‐based surveys are contributing to the dramatic revision of eukaryotic high‐level diversity and phylogeny as the number of sequence data increases. This ongoing revolution gives the opportunity to test for the presence of some eukaryotic taxa in environments where they have not been found using classical microscopic observations. Here, we test whether the foraminifera, a group of single‐celled eukaryotes, considered generally as typical for the marine ecosystems are present in soil. We performed foraminiferal‐specific nested PCR on 20 soil DNA samples collected in contrasted environments. Unexpectedly, we found that the majority of the samples contain foraminiferal SSU rDNA sequences. In total, we obtained 49 sequences from 17 localities. Phylogenetic analysis clusters them in four groups branching among the radiation of early foraminiferal lineages. Three of these groups also include sequences originated from previous freshwater surveys, suggesting that there were up to four independent colonization events of terrestrial and/or freshwater ecosystems by ancestral foraminifera. As shown by our data, foraminifera are a widespread and diverse component of soil microbial communities. Yet, identification of terrestrial foraminiferal species and understanding of their ecological role represent an exciting challenge for future research.     

Phylogeny and Rates of Molecular Evolution of Planktonic Foraminifera: SSU rDNA Sequences Compared to the Fossil Record

Planktonic foraminifera are marine protists, whose calcareous shells form oceanic sediments and are widely used for stratigraphic and paleoenvironmental analyses. The fossil record of planktonic foraminifera is compared here to their molecular phylogeny inferred from ribosomal DNA sequences. Eighteen partial SSU rDNA sequences from species representing all modern planktonic families (Globigerinidae, Hastigerinidae, Globorotaliidae, Candeinidae) were obtained and compared to seven sequences representing the major groups of benthic foraminifera. The phylogenetic analyses indicate a polyphyletic origin for the planktonic foraminifera. The Candeinidae, the Globorotaliidae, and the clade Globigerinidae + Hastigerinidae seem to have originated independently, at different epochs in the evolution of foraminifera. Inference of their relationships, however, is limited by substitution rates of heterogeneity. Rates of SSU rDNA evolution vary from 4.0 × 10⁻⁹ substitutions/site/year in the Globigerinidae to less than 1.0 × 10⁻⁹ substitutions/site/year in the Globorotaliidae. These variations may be related to different levels of adaptation to the planktonic mode of life. A clock-like evolution is observed among the Globigerinidae, for which molecular and paleontological data are congruent. Phylogeny of the Globorotaliidae is clearly biased by rapid rates of substitution in two species (G. truncatulinoides and G. menardii). Our study reveals differences in absolute rates of evolution at all taxonomic levels in planktonic foraminifera and demonstrates their effect on phylogenetic reconstructions. Received: 21 January 1997 / Accepted: 17 April 1997     

Benthic foraminifera at a scallop aquaculture site in Minonosok Bay,the sea of Japan

The species composition and distribution of benthic foraminifera at a scallop aquaculture site in shallow Minonosok Bay (southern Primorye) were studied. Ninety-three species of benthic foraminifera were found in Minonosok Bay in 1998 and 83 species in 2000; representatives of the families Elphidiidae, Discorbidae, Trochamminidae, and Ataxophragmiidae dominated. In 1998, the calcareous species Cribroelphidium frigidum was most abundant; in 2000, calcareous Protelphidium asterotuberculatum and arenaceous species Trochammina inflata and Eggerella advena were dominant. The effect of scallop cultivation on the distribution of benthic foraminifera was local. The species composition and population density of foraminifera directly under scallop cages were decreased, compared to areas of the bay where there were no mariculture operations.