Water temperature affects the physiology of large benthic foraminifers (LBFs) with algal symbionts dwelling in coral reef environments. However, the detailed physiological responses of LBF holobionts to temperature ranges occurring in their habitats are not known. We report net oxygen (O2) production and respiration rates of three LBF holobionts (Baculogypsina sphaerulata and Calcarina gaudichaudii hosting diatom symbionts, and Amphisorus kudakajimensis hosting dinoflagellate symbionts) measured in the laboratory at water temperatures ranging from 5°C to 45°C in 2.5°C or 5°C intervals and with light saturation levels of ∼500 µmol m−2 s−1. In addition, the recovery of net O2 production and respiration rates after exposure to temperature stress was assessed. The net O2 production and respiration rates of the three LBF holobionts peaked at ∼30°C, indicating their optimal temperature for a short exposure period. At extreme high temperatures (≥40°C), the net O2 production rates of all three LBF holobionts declined to less than zero and the respiration rates slightly decreased, indicating that photosynthesis of algal symbionts was inactivated. At extreme low temperatures (≤10°C for two calcarinid species and ≤5°C for A. kudakajimensis), the net O2 production and respiration rates were near zero, indicating a weakening of holobiont activity. After exposure to extreme high or low temperature, the net O2 production rates did not recover until the following day, whereas the respiration rates recovered rapidly, suggesting that a longer time (days) is required for recovery from damage to the photosystem by temperature stress compared to the respiration system. These results indicate that the oxygen metabolism of LBF holobionts can generally cope well with conditions that fluctuate diurnally and seasonally in their habitats. However, temporal heat and cold stresses with high light levels may induce severe damage to algal symbionts and also damage to host foraminifers.
The CO2 concentration of air has increased over the last two centuries and recently surpassed 400 ppm. Carbon cycle models project CO2 concentrations of 720 to 1000 ppm for the IPCC intermediate scenario (RCP 6.0), resulting in an increase in global mean temperature of ~ 2.6 °C and a decrease in seawater pH of ~ 0.3. Together, global warming and ocean acidification are often referred to as the "evil twins" of climate change, potentially inducing severe threats in the near future. In this paper, our discussion is focused on the response of two major calcifiers, foraminifera and corals, which contribute much to the global carbonate burial rate. Photosymbiosis is regarded as an adaptive ecology for living in warm and oligotrophic oceans, especially for reef-building corals and larger reef-dwelling benthic foraminifera. As a consequence of global warming, bleaching may be a global threat to algal symbiont-bearing marine calcifying organisms under conditions of high temperature and light intensity. If CO2 is dissolved in seawater, the partial pressure of CO2 in seawater (pCO2) and dissolved inorganic carbon (DIC) increases while pH and the saturation state of carbonate minerals decreases without any change in total alkalinity. Generally, marine calcifying organisms show decreases in calcification rates in response to acidified seawater. However, the response often differs depending on situations, species, and life-cycle stage. Some benthic foraminifera showed a positive response to low pH conditions. The Acropora digitifera coral calcification of adult branches was not reduced markedly at higher pCO2 conditions, although calcification tended to decrease versus pCO2 in both aposymbiotic and symbiotic polyps. New analytical technologies help identify important constraints on calcification processes. Based upon Ca isotopes, the transport path of Ca2+ and the degree of its activity would predominantly control the carbonate precipitation rate. Visualization of the extracellular pH distribution shows that proton pumping produces the high internal pH and large internal–external pH gap in association with foraminiferal calcification. From the perspective of a long-term change in the Earth's surface environment, foraminifera seem to be more adaptive and robust than corals in coping with ocean warming and acidification but it is necessary to further understand the mechanisms underlying variations in sensitivity to heat stress and acidified seawater for future prediction. Since CO2 is more soluble in lower temperature seawater, ocean acidification is more critical in the polar and high-latitude regions. Additionally, older deep-water has enhanced acidity owing to the addition of CO2 from the degradation of organic matter via a synergistic effect with high pressure. With current ocean acidification, pH and the saturation state of carbonate minerals are decreasing without any change in total alkalinity. However, in the Earth's history, it is well known that alkalinity has fluctuated significantly. Therefore, it is necessary to quantitatively reconstruct alkalinity, which is another key factor determining the saturation state of carbonate minerals. The rapid release of anthropogenic CO2 (in the present day and at the Paleocene/Eocene boundary) induces severe ocean acidification, whereas in the Cretaceous, slow environmental change, even at high levels of pCO2, could raise alkalinity, thereby neutralizing ocean acidification.
Abstract The taxonomic diversity of hermatypic corals decreases with increasing latitude, which correlates with sea‐surface temperatures. However, little is known about latitudinal changes in the taxonomic diversity and biogeographic patterns of larger benthic foraminifera, although their physiological requirements are similar to those of hermatypic corals because of their symbiotic relationships with microalgae. The present study examined how the abundance and taxonomic composition of larger foraminiferal assemblages in shallow‐water reef sediments change with latitude along the Ryukyu Islands (Ryukyus), which are located near the northern limit of coral‐reef distributions in the western Pacific Ocean. Three islands from different latitudes in the Ryukyus were selected to investigate latitudinal changes in larger foraminiferal assemblages: Ishigaki Island (24°20′N, 124°10′E), Kudaka Island (26°09′N, 127°54′E) and Tane‐ga‐shima Island (30°20′N, 131°E). Four sediment samples were taken at each of three topographic sites (beach, shallow lagoon and reef crest) on the reef flat of each island. Foraminiferal tests of a 2.0‐ to 0.5‐mm size fraction were selected, identified and counted. The variations in foraminiferal abundance in reef sediments from three latitudinally different islands exhibit two contrasting trends along reef flats: a shoreward decrease on Ishigaki and Tane‐ga‐shima Islands and a shoreward increase on Kudaka Island. A total of 25, 24 and 13 foraminiferal taxa were identified in Ishigaki, Kudaka and Tane‐ga‐shima Islands, respectively. Baculogypsina sphaerulata , Neorotalia calcar and Amphistegina spp. were dominant (i.e. >3% of foraminiferal assemblages) in the three islands. Calcarina gaudichaudii and Calcarina hispida were common on Ishigaki and Kudaka Islands but were absent on Tane‐ga‐shima Island. Larger foraminiferal assemblages from three different reef‐flat environments on Ishigaki Island can be distinguished, whereas those from the three environments on Kudaka and Tane‐ga‐shima Islands are similar in composition. These latitudinal changes in larger foraminiferal assemblages in reef sediments may possibly be caused by variations in the topography of reef flats, distributions and standing crops of living foraminifers on reef flats, and the northern limit of some calcarinid species in the northern Ryukyus.
Large benthic foraminifera are unicellular calcifying reef organisms that can form symbiotic relationships with a range of different microalgae. However, the cellular functions, such as symbiosis and calcification, and other aspects of cellular physiology in large benthic foraminifera are not fully understood. Amphisorus kudakajimensis was used as a model to determine the detailed cellular characteristics of large benthic foraminifera. We used calcein acetoxymethyl ester (calcein AM) as a fluorescent indicator for live confocal imaging. We demonstrated that calcein AM is a useful fluorescent indicator to stain the fine network of reticulopodia and the cytoplasm in living A. kudakajimensis. We showed that at least two types of reticulopodia exist in A. kudakajimensis: the straight bundle of reticulopodia that spreads from the aperture and the fine reticulopodia along the surface of the aperture and chamber walls. The cytoplasm in outer chambers was highly branched and contained a few dinoflagellates. In contrast, the inner chamberlets contained condensed cytoplasm and many dinoflagellates, suggesting that the cytoplasm of A. kudakajimensis performs different functions based on its location within the large test. Our confocal detailed image analysis provides real-time cellular morphology and cell physiology of living foraminifera.
