Willem Renema

Naturalis Biodiversity Center | NCB · Marine Biodiversity

Reef cores are a powerful tool for investigating temporal changes in reef communities. Radiometric dating facilitates the determination of vertical accretion rates, which has allowed for examination of local-regional controlling factors, such as subsidence and sea level changes. Coral reefs must grow at sufficient rates to keep up with sea level ri...

Molecular techniques like metabarcoding, while promising for exploring diversity of communities, are often impeded by the lack of reference DNA sequences available for taxonomic annotation. Our study explores the benefits of combining targeted DNA barcoding and morphological taxonomy to improve metabarcoding efficiency, using beach meiofauna as a c...

Molecular techniques like metabarcoding, while promising for exploring diversity of communities, are often impeded by the lack of reference DNA sequences available for taxonomic annotation. Our study explores the benefits of combining targeted DNA barcoding and morphological taxonomy to improve metabarcoding efficiency, using beach meiofauna as a c...

Cycloclypeus carpenteri is one of the deepest living large benthic foraminifera. It has an obligatory relationship with diatom photosymbionts, and, in addition, houses a diverse prokaryotic community. Variations in the eukaryotic and prokaryotic endobiotic community composition might be key in allowing Cycloclypeus to occur in low light environment...

Cycloclypeus carpenteri is one of the deepest living large benthic foraminifera. It has an obligatory relationship with diatom photosymbionts, and, in addition, houses a diverse prokaryotic community. Variations in the eukaryotic and prokaryotic endobiotic community composition might be key in allowing Cycloclypeus to occur in low light environment...

Sea surface temperatures (SST) have been identified as a main controlling factor on larger benthic foraminifera (LBF) living in tropical to sub-tropical shallow-water carbonate and mixed siliciclastic‑carbonate platforms. Changes in SST, along with those in ocean acidification and nutrient content recorded in the global oceans throughout their hist...

Plain Language Summary Shells of giant clams exhibit growth bands, similar to tree rings, which form in both seasonal (visible by eye) and daily (resolvable by microscope) increments. However, the optical visibility of daily bands in fossil giant clam shells can be poor. Fortunately, growth bands are often accompanied by changes in the chemical com...

Although Pliocene temperature and pCO2 are similar to those predicted in the IPPC RCP4.5 scenario, the distribution of coral reefs in the center of maximum coral diversity, the Coral Triangle, during this period has not been explored. We discovered a significantly lower occurrence of reefs during the Pliocene, which we refer to as the Pliocene Reef...

Rising atmospheric CO2 shifts the marine inorganic carbonate system and decreases seawater pH, a process often abbreviated to 'ocean acidification'. Since acidification decreases the saturation state for crystalline calcium carbonate (e.g., calcite and aragonite), rising dissolved CO2 levels will either increase the energy demand for calcification...

Mitochondria originated from an ancient bacterial endosymbiont that underwent reductive evolution by gene loss and endosymbiont gene transfer to the nuclear genome. The diversity of mitochondrial genomes published to date has revealed that gene loss and transfer processes are ongoing in many lineages. Most well-studied eukaryotic lineages are repre...

Mitochondria originated from an ancient bacterial endosymbiont that underwent reductive evolution by gene loss and endosymbiont gene transfer to the nuclear genome. The diversity of mitochondrial genomes published to date has revealed that gene loss and transfer processes are ongoing in many lineages. Most well-studied eukaryotic lineages are repre...

Abstract Monitoring community composition of Foraminifera (single‐celled marine protists) provides valuable insights into environmental conditions in marine ecosystems. Despite the efficiency of environmental DNA (eDNA) and bulk‐sample DNA (bulk‐DNA) metabarcoding to assess the presence of multiple taxa, this has not been straightforward for Forami...

Foraminifera are a species-rich phylum of rhizarian protists that are highly abundant in most marine environments. Molecular methods such as metabarcoding have revealed a high, yet undescribed diversity of Foraminifera. However, so far only one molecular marker, the 18S ribosomal RNA, was available for metabarcoding studies on Foraminifera. Primers...

Only two alveolinoid genera, Borelis de Montfort, 1808 and Alveolinella H. Douvillé, 1907 thrive in present-day Indo-Pacific coral-reef settings. The former is widespread from the Western (Red Sea) to the Central Indo-Pacific and Caribbean Sea coasts, whereas the latter occurs in the Central and Eastern Indo-Pacific area. A third Indo-Pacific alveo...

Traditional morphological methods for species identification are highly time consuming, especially for small organisms, such as Foraminifera, a group of shell-building microbial eukaryotes. To analyze large amounts of samples more efficiently, species identification methods have extended to molecular tools in the last few decades. Although a wide r...

Foraminifera are a species-rich phylum of rhizarian protists that are highly abundant in many marine environments and play a major role in global carbon cycling. Species recognition in Foraminifera is mainly based on morphological characters and nuclear 18S ribosomal RNA barcoding. The 18S rRNA contains variable sequence regions that allow for the...

Miocene, Austrotrillina Parr, 1942 is the only genus showing a non-homogeneous shell structure. This consists of a parakeriotheca, coated by a thin, dense tectum. Four Austrotrillina species (A. brunni, A. eocaenica, A. howchini, A. striata) have been often used as biostratigraphical markers in the Mediterranean and Indo-Pacific areas. New material...

Meiofaunal animals, roughly between 0.045 and 1 mm in size, are ubiquitous and ecologically important inhabitants of benthic marine ecosystems. Their high species richness and rapid response to environmental change make them promising targets for ecological and biomonitoring studies. However, diversity patterns of benthic marine meiofauna remain po...

Abstract Background Understanding the specificity and flexibility of the algal symbiosis-host association is fundamental for predicting how species occupy a diverse range of habitats. Here we assessed the algal symbiosis diversity of three species of larger benthic foraminifera from the genus Amphistegina and investigated the role of habitat and sp...

Ocean acidification is expected to impact the high latitude oceans first, as CO2 dissolves more easily in colder waters. At the current rate of anthropogenic CO2 emissions, the sub-Antarctic Zone will start to experience undersaturated conditions with respect to aragonite within the next few decades, which will affect marine calcifying organisms. S...

Oxygen-depleted regions of the global ocean are rapidly expanding, with important implications for global biogeochemical cycles. However, our ability to make projections about the future of oxygen in the ocean is limited by a lack of empirical data with which to test and constrain the behavior of global climatic and oceanographic models. We use dep...

Shelled pteropods are widely regarded as bioindicators for ocean acidification, because their fragile aragonite shells are susceptible to increasing ocean acidity. While short-term incubations have demonstrated that pteropod calcification is negatively impacted by ocean acidification, we know little about net calcification in response to varying oc...

Foraminifera are a group of mostly marine protists with high taxonomic diversity. Species identification is often complex, as both morphological and molecular approaches can be challenging due to a lack of unique characters and reference sequences. An integrative approach combining state of the art morphological and molecular tools is therefore pro...

Ocean gateways facilitate circulation between ocean basins, thereby impacting global climate. The Indonesian Gateway transports water from the Pacific to the Indian Ocean via the Indonesian Throughflow (ITF) and drives the strength and intensity of the modern Leeuwin Current, which carries warm equatorial waters along the western coast of Australia...

Oxygen-depleted regions of the global ocean are rapidly expanding, with important implications for global biogeochemical cycles. However, our ability to make projections of a future deoxygenated ocean is limited by a lack of empirical data with which to test and constrain the behavior of global climatic and oceanographic models. We use depth-strati...

Zooplankton are key players in marine ecosystems, linking primary production to higher trophic levels. The high abundance and high taxonomic diversity renders zooplankton ideal for biodiversity monitoring. However, taxonomic identification of the zooplankton assemblage is challenging due to its high diversity, subtle morphological differences and t...

Understanding the role of dispersal and adaptation in the evolutionary history of marine species is essential for predicting their response to changing conditions. We analyzed patterns of genetic differentiation in the key tropical calcifying species of large benthic foraminifera Amphistegina lobifera to reveal the evolutionary processes responsibl...

Background Revealing the specificity and flexibility of the algal symbiont-host association is fundamental for understanding how species can occupy a diverse range of habitats. Here we assessed the global distribution of the algal symbiont diversity for three shallow-water species of large benthic foraminifera (LBF) of the genus Amphistegina . Spec...

Planktonic foraminifera grow by adding chambers onto their tests, modifying their surface area, volume, porosity, and ornamentation with each addition. This process results in a wide variety of adult morphologies and preserves a record of the early morphology. With high-resolution three-dimensional imaging techniques, precise measurements can be ma...

PCR-free techniques such as meta-mitogenomics (MMG) can recover taxonomic composition of macroinvertebrate communities, but suffer from low efficiency, as >90% of sequencing data is mostly uninformative due to the great abundance of nuclear DNA that cannot be identified with current reference databases. Current MMG studies do not routinely check da...

A previously undocumented, diverse assemblage of very shallow-water larger benthic foraminifera (LBF) is described from the Panna-Mukta fields, offshore India. This location lies at the margin of the late Eocene to early Miocene Arabian Peninsula marine biodiversity hotspot. The assemblage has similar characteristics to those from the Middle East,...

Large benthic foraminifera (LBF) are an important component of low-light, mesophotic tropical marine environments, including coral ecosystems. LBF occur from nearshore, shallow coastal environments experiencing high-terrestrial runoff to the deep-shelf edge in transparent, oceanic waters. Here, I compare the LBF in both these low-light habitats. In...

Benthic foraminifera, and certainly symbiont-bearing (large) benthic foraminifera are generally considered to have large geographic ranges in combination with significant ecomorphological variation. With the advance of molecular phylogenetic approaches, supported or preceded by detailed morphological studies, it was demonstrated that this view need...

Morphological measurements used in this study. (XLSX)

Large benthic Foraminifera (LBF) are major carbonate producers on coral reefs, and are hosts to a diverse symbiotic microbial community. During warm episodes in the geological past, these reef‐building organisms expanded their geographical ranges as subtropical and tropical belts moved into higher latitudes. During these range‐expansion periods, LB...

The clustering of mitochondria near pores in the test walls of foraminifera suggests that these perforations play a critical role in metabolic gas exchange. As such, pore measurements could provide a novel means of tracking changes in metabolic rate in the fossil record. However, in planktonic foraminifera, variation in average pore area, density,...

The clustering of mitochondria near pores in the test walls of foraminifera suggests that these perforations play a critical role in metabolic gas exchange. As such, pore measurements could provide a novel means of tracking changes in metabolic rate in the fossil record. However, in planktonic foraminifera, variation in pore size, density, and poro...

Significance Reconstructing the degree of warming during geological periods of elevated CO 2 provides a way of testing our understanding of the Earth system and the accuracy of climate models. We present accurate estimates of tropical sea-surface temperatures (SST) and seawater chemistry during the Eocene (56–34 Ma before present, CO 2 >560 ppm). T...

To provide a comprehensive palaeoenvironmental reconstruction based on larger benthic foraminifera (LBF), a quantitative analysis of their assemblage composition is needed. Besides microfacies analysis which includes environmental preferences of foraminiferal taxa, statistical analyses should also be employed. Therefore, de-trended correspondence a...

Large benthic foraminifera (LBF) are important components of tropical shallow-marine ecosystems, in which they are abundant on both coral reefs and in the inter-reef areas. These protists are, similar to reef-building corals, photosymbiotic, restricted to warm (> 14 °C) seawater temperatures, and to benthic habitats within the photic zone. Because...

AimCenozoic dynamics of large-scale species diversity patterns remain poorly understood, especially for the Western Pacific, in part, because of the paucity of well-dated fossil records from the tropics. This article aims to reveal the spatiotemporal dynamics of species diversity in the Western Pacific through the Cenozoic, focusing on the tropical...

Late Miocene to mid-Pleistocene sedimentary proxy records reveal that northwest Australia underwent an abrupt transition from dry to humid climate conditions at 5.5 million years (Ma), likely receiving year-round rainfall, but after ~3.3 Ma, climate shifted towards an increasingly seasonal precipitation regime. The progressive constriction of the I...

Global climate underwent a major reorganization when the Antarctic ice sheet expanded ~14 million years ago (Ma) (1). This event affected global atmospheric circulation, including the strength and position of the westerlies and the Intertropical Convergence Zone (ITCZ), and, therefore, precipitation patterns (2–5). We present new shallow-marine sed...

The transition from the Bartonian to the Priabonian, as traditionally understood, has long been associated with a series of extinctions and originations in several microfossil groups. The planktonic forami-nifer genus Morozovelloides and large species of Acarinina suffered a rapid global extinction, as did many radiolarians. Calcareous nannofossils...

Biodiversity hotspots are increasingly recognized as areas of high taxonomic and functional diversity. These hotspots are dynamic and shift geographically over time in response to environmental change. To identify drivers of the origin, evolution, and persistence of diversity hotspots, we investigated the diversity patterns of reef-building corals...

Little is known about Miocene climate in the southeast Indian Ocean, off Western Australia. International Ocean Discovery Program (IODP) Expedition 356: Indonesian Throughflow drilled a latitudinal transect of sites along the modern shelf to investigate paleoclimatic and paleoceanographic conditions. We present lithologic evidence for aridity and c...

The transition from the Bartonian to the Priabonian, as traditionally understood, has long been associated with a series of extinctions and originations in several microfossil groups. The planktonic forami- nifer genus Morozovelloides and large species of Acarinina suffered a rapid global extinction, as did many radiolarians. Calcareous nannofossil...

As one of the most prolific and widespread reef builders, the staghorn coral Acropora holds a disproportionately large role in how coral reefs will respond to accelerating anthropogenic change. We show that although Acropora has a diverse history extended over the past 50 million years, it was not a dominant reef builder until the onset of high-amp...

Studies on ancient coral communities living in marginal conditions, including low light, high turbidity, extreme temperatures, or high nutrients, are important to understand the current structure of reefs and how they could potentially respond to global changes. The main goal of this study was to document the rich and well-preserved fossil coral fa...

Coral patch reefs in the Miocene Mahakam delta in East Kalimantan (Borneo, Indonesia) developed in shallow marine turbid waters. These reefs grew in delta front to prodelta environments under fluctuating siliciclastic input. Langhian patch reefs are well exposed in limestone quarries of the Air Putih area, near the city of Samarinda and include two...

The Maikop Series forms an important source rock in the former Paratethys. Deposition is often interpreted as anoxic, linked to restriction of the Paratethys. The Pirembel formation in the Talysh Mountains (Azerbaijan) is attributed to the Maikop Series and was deposited above the Eocene volcanic Peshtasar formation. Dating the onset of anoxia coul...

Reticulate Nummulites are a widespread and distinctive group of Nummulites, frequently used in biostratigraphy, but their evolution is poorly understood. Studies from the Western Tethys suggest they form a single lineage, the Nummulites fabianii lineage, with an increasing proloculus size over time. This has led to their use as one of the diagnosti...

Assemblages of corals, sponges, foraminifera, sediment bacteria and sediment archaea were assessed at two depths in the Spermonde Archipelago. Our goal was to assess to what extent variation in composition could be explained by habitat and water quality variables. The habitat variables consisted of depth, substrate type and scleractinian coral cove...

Larger benthic foraminifera (LBF) are important and prolific carbonate producers both in modern and ancient shallow tropical seas. During the Paleogene the genus Nummulites was particularly abundant with a global distribution, leading it to be frequently used in biostratigraphy. However, their evolution is poorly understood as classification is Eur...

Larger benthic foraminifera (LBF) are an important tool for the biostratigraphy of (sub)tropical shallow marine deposits. In Paleogene the genus Nummulites is an important genus for biostratigraphical zonation schemes. However, classification is Europe centered and based on external characters and equatorial thin sections. New results from regions...

Larger benthic foraminifera (LBF) are an important tool for the biostratigraphy of (sub)tropical shallow marine deposits. In Paleogene the genus Nummulites is an important genus for biostratigraphical zonation schemes. However, classification is Europe centered and based on external characters and equatorial thin sections. New results from regions...

Accurate assessment of location and timing of speciation of species is needed to discriminate between macroevolutionary models explaining large scale biodiversity patterns. In this paper I evaluate fossil evidence of variation in geographical ranges through time, as well as spatio-temporal variation in morphological parameters to examine geographic...

Seagrass meadows are important shallow-water ecosystems that provide habitat for numerous associated organisms and play a crucial role in nutrient cycling, but their detection in the fossil record is problematic. Indirect indicators are often needed to discriminate seagrass beds from other shallow marine paleohabitats. Here, the stable isotope sign...

This study is a preliminary assessment of an extremely diverse Tortonian (late Miocene) mollusk assemblage from a coral carpet environment preserved at Bontang (East Kalimantan, Indonesia). Even though coral-associated aragonitic faunas are rarely well preserved, the composition of the assemblage described here can be used to address the following...

Study of the extinct and extant biota of the Coral Triangle region has not yet provided answers to questions about mechanisms controlling the origins and maintenance of this marine biodiversity hotspot. We present an updated stratigraphy and revise the taxonomic determinations for important historical collections from Indonesia that have been the b...