BFORAMS@MIKROTAX: AN ONLINE DATABASE FOR DEEP-SEA BENTHIC FORAMINIFERAL TAXONOMY

Accurate identification of microfossils is the foundation for qualitative and quantitative studies of their assemblages as well as for reliable geochemical analyses of their tests. In turn, this is the basis for paleoenvironmental, paleoceanographic, and paleoclimatic as well as biostratigraphic and paleobiological inferences. The development of the databases nannotax (from 2007; Young et al., 2019) and pforams@mikrotax (from Huber et al., 2016) by the user community enabled researchers to make major advances in understanding the taxonomy and evolution of these organisms. These databases provide a single, easily accessible resource for taxonomy experts who otherwise would need to consult multiple publications that are not always accessible and can be used by researchers compiling large datasets (e.g., for evaluating changes in global diversity over time, or researching species’ provinciality and bathymetry). One of the major benefits of databases such as these is the improved stability in taxonomic identifications and nomenclature. In addition, the databases have been proven useful in training early career scientists in nannofossil and planktonic foraminiferal taxonomy and are routinely used by researchers without formal taxonomic training who analyze microfossils for geochemistry-focused investigations.

In the summer of 2022, taxonomic experts and early career scientists established the benthic foraminiferal working group with the goal of building a similar, universally accessible, high-quality online taxonomic database of Cretaceous through Cenozoic benthic foraminifera (indicated in Table 1). This spans time periods for which a wealth of data is available from ocean drilling programs. The first phase of building the “bforams” database focused on deep-sea benthic foraminifera because they mostly consist of widely documented, cosmopolitan species and are most frequently used in geochemical studies. The bforams@mikrotax database (https://www.mikrotax.org/bforams/bf-pages/bf-citation.html; Young & Huber, 2024) uses the same software systems as the successful nannotax and pforams@mikrotax databases and is organized similarly. Now available online, bforams@mikrotax is developing into a rigorously revised taxonomic compilation that includes taxonomic descriptions, images, citations, and expert opinions.

Benthic foraminifera are shell-forming, single-celled organisms that are found widely across all ocean environments. They are used to reconstruct seafloor environments as they are abundant and show species- and population-level responses to changes in their environments, likely as a result of their short life spans (Ohga & Kitazato, 1997). Benthic foraminifera are common in marine sediments and are extensively used in paleoceanographic, paleoecologic, paleoclimatologic, and biostratigraphic research as well as in evolutionary lineage research (Gooday, 2003; Sen Gupta, 2003; Jorissen et al., 2007; Murray, 2007). Studies of benthic foraminiferal assemblages and stable isotope and trace elemental analyses of their tests (shells) are commonly used to reconstruct paleobathymetry, deep-sea temperature, ocean circulation, organic carbon flux (thus nutrient content and carbonate saturation), bottom or pore water oxygenation levels, pH, and continental ice volume (e.g., Katz et al., 2010; Schmiedl, 2019). Examples of geochemical measurements performed on calcareous benthic foraminiferal species, and applied as paleoceanographic proxies, are stable oxygen (δ¹⁸O), carbon (δ¹³C), nitrogen (δ¹⁵N), and boron (δ¹¹B) isotopes, and trace element to calcium ratios (e.g., Mg-Na-Li-Sr-B-Cd-U-Zn-I-S/Ca; Katz et al., 2010; Westerhold et al., 2020; Pacho et al., 2023 and references therein). The relevance of benthic foraminiferal reconstructions is highlighted by the IPCC 6^th Assessment Report (Lee et al., 2023), which compared Cenozoic atmospheric CO₂ with temperature reconstructions based on δ¹⁸O benthic foraminiferal proxy reconstructions, and Hansen et al. (2008), who used the Cenozoic δ¹⁸O benthic foraminiferal record as the primary basis for establishing 350 ppmv atmospheric pCO₂ as a target for efforts to control future global warming.

Benthic foraminiferal species must be accurately identified for geochemical studies because different species living in the same environment may have different sensitivities and reactions to environmental parameters. Different species of benthic foraminifera occupy a range of microhabitats that determine the water chemistry that they are exposed to, which influences the isotope (e.g., McCorkle et al., 1990; Mackensen et al., 2000; Fontanier et al., 2006) and trace metal incorporation into foraminiferal tests (e.g., Tachikawa & Elderfield 2002; Koho et al., 2017). Furthermore, there are differences among species and individuals in how they take in elemental and isotopic material (see vital effect discussions in e.g., Erez, 1978; Grossman, 1987; Hintz et al., 2006). Therefore, mixing more than one species in a geochemical analysis may result in skewed paleoclimatic and paleoceanographic interpretations. Accurate taxonomic identification is fundamental to generating reliable geochemical data, enabling scientists to discern subtle shifts in ocean chemistry over geological timescales. This information enhances our understanding of Earth’s history and also contributes to predictions about future climate trends and oceanic responses to global environmental changes.

Benthic foraminifera are arguably the most numerous and diverse fossilized organisms in the largest habitat on Earth—the deep-sea floor (Gooday, 2003). Evidence from DNA sequencing indicates they originated in the late Proterozoic (Wray et al., 1995), whereas the earliest known unequivocal foraminifera were identified in the Lower Cambrian (Culver, 1991). Benthic foraminifera are much more species-rich and morphologically disparate in living populations than their planktonic counterparts. Estimates of the number of extant benthic foraminiferal species diversity vary from 2,140 (Murray, 2007) to 6,700 (Pawlowski et al., 2014) species, and to as many as 10,000 (Adl et al., 2007) species, with the latter number including naked species, which are more diverse than living species with tests (e.g., Lecroq et al., 2011). In contrast, there are no more than 50 extant species and subspecies of planktonic foraminifera (Brummer & Kučera, 2022). All planktonic foraminifera are placed within the Order Rotaliida, which contains most of the extant calcareous benthic foraminiferal species, and the clade of the Globothalamea (e.g., Morard et al., 2022; de Nooijer et al., 2023). In contrast to planktonic foraminifera, which all have calcitic, perforate tests, benthic foraminifera either lack tests, produce agglutinated tests, or secrete calcareous (perforate, or imperforate) calcitic or aragonitic tests (e.g., Tappan & Loeblich, 1988; Loeblich & Tappan, 1988; Pawlowski et al., 2013; de Nooijer et al., 2023), or (rarely) siliceous tests or composite calcareous/siliceous tests (Borrelli et al., 2018; Richirt et al., 2024).

The compilation of ocean drilling taxonomic data in the extending Ocean Drilling Pursuits (eODP) project has listed 1,528 benthic foraminiferal “distinct taxonomic entries”, which represents about 33% of taxonomic entries for all microfossil groups recognized at deep sea drill sites (Sessa et al., 2023). The Ellis & Messina (1940) catalog of primary types contains about 47,000 entries of fossil and extant benthic foraminiferal species, without consideration of taxonomic synonymy. The World Foraminifera Database—accessible via the World Register of Marine Species (WoRMS)—at the time of writing, has 8,961 valid extant species and 40,971 valid fossil benthic foraminiferal species, for a total of 49,036 validated species (Hayward et al., 2022). The information collected in the WoRMS database provides an excellent record of taxonomic classification, species validity, synonymized names, taxonomic and phylogenic inferences, and taxonomic literature. However, this database lacks illustrations, images, discussion of morphological variability within and among species, information on stratigraphic ranges and ecological preferences, the range of morphologies, and a searchable option based on morphologic features. This limits the applicability of WoRMS as a routine tool for non-expert researchers. Similarly, the benthic foraminiferal data in the eODP compilation have been taxonomically evaluated to some extent, but they do not contain species descriptions or images (Sessa et al., 2023).

Benthic foraminiferal species identifications can be challenging, given the high number of species described and the complexity of identifying species based on key morphologic features. Barriers such as an unfamiliarity with morphologic terminology and with the language of the species description, inaccessibility of original species descriptions, contradictory information among different monographs, and a lack of quality and diversity of images of type and additional specimens can lead to frustration and misidentifications. The bforams@mikrotax database seeks to serve as a user-friendly repository for Scanning Electron Microscope (SEM) and light microscopy images, morphologic descriptions (both accepted and original), ecologic distributions, and stratigraphic occurrences. While these elements are key components of the database, we anticipate that the database will also become a catalyst for new scientific insights following meaningful discussions within the scientific community. By providing diverse and reliable images alongside detailed morphologic descriptions, our platform aims to stimulate dialogue surrounding naming schemes, synonymy issues, and other pertinent topics. By fostering open discourse and collaboration, we can enhance our understanding of benthic foraminifera, improve stability in taxonomic identifications and nomenclature, enable better use of global foraminiferal databases, and contribute to advancements in the field.

The bforams@mikrotax database is composed of two interlinked catalogs that serve different functions. The “Main Database” provides a synthesis of currently accepted taxonomic concepts together with information on their nomenclature and synonymies, distribution data, and high-quality images. It identifies recent taxonomic revisions, images, and expert opinions. The “Original Description Catalog” provides a reference listing of described species, irrespective of their acceptance or validity, including type figures, and original diagnoses. Where access to the original literature is problematic, much of this content is sourced from the Ellis & Messina catalog. The bforams@mikrotax database is searchable via words or stylized drawings that allow users to choose any combination of morphologic features, depth habitat, stratigraphic range and taxonomy, and it contains images, species descriptions, and information reported in the original species descriptions to assist both experts and non-experts in foraminiferal identifications. A database of this kind is essential for retention of knowledge and maintaining expertise in a field where retirements and academic turnover are common (e.g., Bik, 2017).

Taxonomic opinions are constantly evolving, and the database will need to be continually updated. User input will serve to identify areas of controversy as well as taxonomic concepts in need of revision. In this context, the database will provide a platform for discussions that should spark further investigations and identify topics for research. Moreover, the bforams@mikrotax database will incorporate results of the most recent investigations into phylogenetics of living species, which connect biological and genetically based species or taxonomic group concepts that are not easily determined based only on morphologic approaches. Since the 1990s, genetic sequencing of benthic foraminifera has led to major revisions of supra-specific taxonomy of benthic foraminifera (e.g., Wray et al., 1993, 1995; Pawlowski et al., 2013; de Nooijer et al., 2023). The benthic foraminiferal online database will facilitate a more complete understanding of evolutionary lineages/event timings and will engage the interest of the broader (paleo)biological community.

With ∼1,600 benthic foraminiferal taxon records in the main database and 3,000 images now available, including some of the most common species and species most frequently used for geochemistry, bforams@mikrotax is in its initial growth phase as a reference source. Like pforams@mikrotax, this resource will be of particular interest to the International Ocean Discovery Program (IODP) research community and will be invaluable in extending the information in eODP, which has compiled IODP materials from over a thousand holes and includes benthic foraminiferal records (Sessa et al., 2023). The input of taxonomic descriptions and related image formatting has been achieved through the volunteer efforts of many contributors.

Taxonomic and phylogenetic uncertainties have been discussed and debated among multiple working subgroups composed of taxonomic experts to try and reach (for now) final decisions on nomenclature and synonymies. The opinions of the subgroup members are documented and included on each species’ page. The subgroups will continue to monitor opinions and comments submitted by the user community through the Mikrotax comment field. After reviewing comments, the subgroup will make a recommendation to the working group for a final decision on whether a revision of the Main Catalog entry is necessary. As new taxonomic and phylogenetic revisions are published, the new species will be added to the Original Species Catalog, and the Main Catalog will be updated based on consensus of the working group, with decisions and rationales stated in the “Remarks” section on the species pages. Monographs presently in the database include Hayward et al. (2012), Holbourn et al. (2013), Holbourn & Kaminski (1997), Alegret & Thomas (2001), Katz et al. (2003), Tjalsma & Lohmann (1983), and van Morkhoven et al. (1986).

The Main Database contains pages of foraminifera of accepted species names only (Fig. 1), with priority for inclusion given to the most ubiquitous, commonly identified Cenozoic through Cretaceous taxa found in deep-sea sediments and those considered as important for paleoceanographic research. This time period includes the major radiation of Rotaliid taxa (calcite, perforate; Tappan & Loeblich, 1988; Loeblich & Tappan, 1988), with the majority of documented species belonging to that clade.

Most species’ records include multiple light and/or SEM images illustrated from one or more published sources to show different views of the test for primary and secondary type specimens. Each record also includes a character matrix of key morphological characters, an age-range graphic, and bathymetric distribution summary. The character matrix provides the framework for the Advanced Search feature that allows users to search the database by key morphologic features (see Advanced Search Menu section below). If a species has been the topic of discussion, the Main Catalog page also contains a Working Group Opinion statement to clarify conflicting information.

A “taxon-table”, which provides a listing of the included sub-taxa with representative images and concise statements of their distinguishing features, is a special feature of the database for higher taxa (genera and above; Fig. 2). This table provides a convenient way to browse the database graphically, and it provides a pathway for new users to learn and understand the taxonomic classification of benthic foraminifera.

The “Original Description Catalog” is a comprehensive catalog of described benthic foraminifera, providing verbatim copies of original descriptions and remarks, and original illustrations of type specimens (Fig. 3). These pages also include descriptions (some of which required English-language translations) and images extracted from the Ellis & Messina (1940) catalogs. There is an ongoing effort to obtain new SEM images and extended depth focus (EDF) micrographs of primary types (holotypes, paratypes, neotypes, lectotypes, and syntypes), with an emphasis on species that are considered valid. This effort enables further clarification of species concepts, as many species, especially those described long ago, were poorly illustrated in their original publications. In addition to the original descriptions, information in the Original Description Catalog includes original and currently used genus and species name combinations, the authors and dates for species names, primary type specimen dimensions, type locality and age, repository information, and bibliographic references. Links to the Main Catalog, a taxon search box, and multiple drop-down links allow for easy navigation to other parts of the database from the Original Description Catalog. The database facilitates convenient quick searches using the taxon name window at the top and bottom of every page. The landing page for each species contains browsable images and sister taxa that are linked to subsequent pages for quick access.

The Advanced Search form (Fig. 4) can be used as an aid to species identification by selecting key morphological features grouped in four categories (test shape, chamber arrangement, surface features, aperture). By clicking on a combination of morphologic features in a specimen, this search tool provides a list with thumbnail images of the species that fit the input criteria; the researcher can then peruse those options for the best match to the specimen that needs identification. When the geologic age sliding scale bar is selected on the advanced search menu, only taxa occurring within the selected time interval will be displayed in the search results. Results can also be filtered by depth zone, wall type, or taxonomic criteria. These search functions will enable rapid species identification and quick access to information on biogeographic, paleoenvironmental, bathymetric and biostratigraphic distributions.

As the working group nears completion of first phase goals, additional published monographs are being considered for incorporation into the database. Decisions on subsequent taxonomic revisions to incorporate in the database will be based on the majority opinions of the working group and will be influenced by public comments, meeting discussions, and published morphometric and genetic data. For micropaleontology experts participating in the IODP or potential future successors, it is likely that bforams@mikrotax will become the primary resource to assist in identifying species. Additionally, the database will be essential to the research community by providing updated taxonomic concepts and biostratigraphic and environmental ranges.

To continue this work, members of the working group (Table 1) will seek funding to support group meetings, enable high resolution imaging of museum collections, perform morphological assessments of key taxa, and encourage conversations and debates on the global, regional, bathymetric, and environmental distributions of species through time. The bforams@mikrotax initiative is working to coordinate incorporation of MicroCT scans of specimens (especially primary types) into the bforams@mikrotax database; some are already available from the collections in the American Museum of Natural History. Support to maintain and grow working group membership and activities will be facilitated by bringing in more colleagues from academia and industry and by increasing taxonomic and stratigraphic expertise. The database has been presented at The Micropalaeontological Society Annual Conference 2022 (Bremen, Germany; Alegret et al., 2022) and at the FORAMS 2023 international conference on foraminifera (Perugia, Italy), increasing its exposure and membership. This growing community will facilitate consistent updating and expansion of the bforams@mikrotax database.

Thanks to all the members of the bforams@mikrotax initiative (Table 1) and to Corinne Church (George Mason University) for her outstanding volunteer work adding text and images to to the original description catalog. The U.S. Science Support Program (USSSP) sponsored a workshop to develop this online taxonomic database for deep-sea benthic foraminifera. Those who attended this workshop at the Smithsonian National Museum of Natural History in August 2023 were essential to the successful development of this database. The UK Natural Environment Research Council funded development of the nannotax and pforams@mikrotax databases, including development of the database system used by bforams@mikrotax. We are especially grateful to Micropaleontology Press for making the Ellis & Messina catalog available to us for incorporation into the bforams@mikrotax database.