Articles | Volume 14, issue 4
Research article 28 Feb 2017
Research article | 28 Feb 2017
Cyanobacterial endobionts within a major marine planktonic calcifier (Globigerina bulloides, Foraminifera) revealed by 16S rRNA metabarcoding
Clare Bird et al.
No articles found.
Jeroen Groeneveld, Helena L. Filipsson, William E. N. Austin, Kate Darling, David McCarthy, Nadine B. Quintana Krupinski, Clare Bird, and Magali Schweizer
J. Micropalaeontol., 37, 403–429,Short summary
Current climate and environmental changes strongly affect shallow marine and coastal areas like the Baltic Sea. The combination of foraminiferal geochemistry and environmental parameters demonstrates that in a highly variable setting like the Baltic Sea, it is possible to separate different environmental impacts on the foraminiferal assemblages and therefore use chemical factors to reconstruct how seawater temperature, salinity, and oxygen varied in the past and may vary in the future.
Raphaël Morard, Franck Lejzerowicz, Kate F. Darling, Béatrice Lecroq-Bennet, Mikkel Winther Pedersen, Ludovic Orlando, Jan Pawlowski, Stefan Mulitza, Colomban de Vargas, and Michal Kucera
Biogeosciences, 14, 2741–2754,Short summary
The exploitation of deep-sea sedimentary archive relies on the recovery of mineralized skeletons of pelagic organisms. Planktonic groups leaving preserved remains represent only a fraction of the total marine diversity. Environmental DNA left by non-fossil organisms is a promising source of information for paleo-reconstructions. Here we show how planktonic-derived environmental DNA preserves ecological structure of planktonic communities. We use planktonic foraminifera as a case study.
Catherine V. Davis, Tessa M. Hill, Ann D. Russell, Brian Gaylord, and Jaime Jahncke
Biogeosciences, 13, 5139–5150,Short summary
We examine seasonality of planktic foraminifera in an upwelling area to identify species vulnerable to changes in upwelling and ocean acidification and improve interpretation of fossil foraminifera. Of species associated with upwelling on the central California shelf, some are consistent with observations elsewhere while some associations appear to be unique to the region. All species show lunar periodicity and we confirm the presence of foraminifera at very low saturation state of calcite.
T. Bush, I. B. Butler, A. Free, and R. J. Allen
Biogeosciences, 12, 3713–3724,Short summary
Despite their global importance, redox reactions mediated by microorganisms are often crudely represented in biogeochemical models. We show that including the dynamics of microbial growth in such a model can cause sudden shifts between redox states in response to an environmental change. We identify the conditions required for these redox regime shifts, and predict that they are likely in the modern day sulfur and nitrogen cycles, and potentially the iron cycle in the ancient ocean.
C. V. Davis, M. P. S. Badger, P. R. Bown, and D. N. Schmidt
Biogeosciences, 10, 6131–6139,
Related subject area
Biodiversity and Ecosystem Function: MarineEffects of spatial variability on the exposure of fish to hypoxia: a modeling analysis for the Gulf of MexicoPlant genotype determines biomass response to flooding frequency in tidal wetlandsFactors controlling the competition between Phaeocystis and diatoms in the Southern Ocean and implications for carbon export fluxesCharacterization of particle-associated and free-living bacterial and archaeal communities along the water columns of the South China SeaAdult life strategy affects distribution patterns in abyssal isopods – implications for conservation in Pacific nodule areasDiversity and distribution of nitrogen fixation genes in the oxygen minimum zones of the world oceansStructure and function of epipelagic mesozooplankton and their response to dust deposition events during the spring PEACETIME cruise in the Mediterranean SeaIdeas and Perspectives: When ocean acidification experiments are not the same, reproducibility is not testedReview and syntheses: Turbidity flows – evidence for effects on deep-sea benthic community productivity is ambiguous but the influence on diversity is clearerDistribution of planktonic foraminifera in the subtropical South Atlantic: depth hierarchy of controlling factorsTechnical note: Estimating light-use efficiency of benthic habitats using underwater O2 eddy covarianceThe effect of salinity, light regime and food source on C and N uptake in a kleptoplast-bearing foraminiferaOcean acidification reduces growth and grazing impact of Antarctic heterotrophic nanoflagellatesDynamics of environmental conditions during the decline of a Cymodocea nodosa meadowMegafauna community assessment of polymetallic-nodule fields with cameras: platform and methodology comparisonA meta-analysis on environmental drivers of marine phytoplankton C : N : PSpatial and temporal variability in the response of phytoplankton and prokaryotes to B-vitamin amendments in an upwelling systemBiogeography and community structure of abyssal scavenging Amphipoda (Crustacea) in the Pacific OceanAre seamounts refuge areas for fauna from polymetallic nodule fields?Ocean deoxygenation and copepods: coping with oxygen minimum zone variabilityUnexpected high abyssal ophiuroid diversity in polymetallic nodule fields of the northeast Pacific Ocean and implications for conservationPopulation dynamics of modern planktonic foraminifera in the western Barents SeaForaminiferal community response to seasonal anoxia in Lake Grevelingen (the Netherlands)Changes in population depth distribution and oxygen stratification explain the current low condition of the Eastern Baltic Sea cod (Gadus morhua)Light availability modulates the effects of warming in a marine N2 fixerSiR-actin-labelled granules in foraminifera: patterns, dynamics, and hypothesesAlpha and beta diversity patterns of polychaete assemblages across the nodule province of the eastern Clarion-Clipperton Fracture Zone (equatorial Pacific)Dimensions of marine phytoplankton diversityThe Arctic picoeukaryote Micromonas pusilla benefits from ocean acidification under constant and dynamic lightFlux variability of phyto- and zooplankton communities in the Mauritanian coastal upwelling between 2003 and 2008Environmental factors influencing benthic communities in the oxygen minimum zones on the Angolan and Namibian marginsHypoxia in mangroves: occurrence and impact on valuable tropical fish habitatCalcification and latitudinal distribution of extant coccolithophores across the Drake Passage during late austral summer 2016Distribution of free-living marine nematodes in the Clarion–Clipperton Zone: implications for future deep-sea mining scenariosCharacterizing photosymbiosis in modern planktonic foraminiferaIdentifying areas prone to coastal hypoxia – the role of topographyObservations of deep-sea fishes and mobile scavengers from the abyssal DISCOL experimental mining areaOcean acidification and high irradiance stimulate the photo-physiological fitness, growth and carbon production of the Antarctic cryptophyte Geminigera cryophilaRates and drivers of Red Sea plankton community metabolismReviews and syntheses: Insights into deep-sea food webs and global environmental gradients revealed by stable isotope (δ15N, δ13C) and fatty acid trophic biomarkersLight-dependent calcification in Red Sea giant clam Tridacna maximaResponses of an abyssal meiobenthic community to short-term burial with crushed nodule particles in the south-east PacificA trait-based modelling approach to planktonic foraminifera ecologyPhysiological and biochemical responses of Emiliania huxleyi to ocean acidification and warming are modulated by UV radiationEnhanced microbial nitrogen transformations in association with macrobiota from the rocky intertidalMeso-zooplankton structure and functioning in the western tropical South Pacific along the 20th parallel south during the OUTPACE survey (February–April 2015)Impact of carbonate saturation on large Caribbean benthic foraminifera assemblagesFactors influencing test porosity in planktonic foraminiferaCoral reef carbonate budgets and ecological drivers in the central Red Sea – a naturally high temperature and high total alkalinity environmentThe ability of macroalgae to mitigate the negative effects of ocean acidification on four species of North Atlantic bivalve
Elizabeth D. LaBone, Kenneth A. Rose, Dubravko Justic, Haosheng Huang, and Lixia Wang
Biogeosciences, 18, 487–507,Short summary
The hypoxic zone is an area of low dissolved oxygen (DO) in the Gulf of Mexico. Fish can be killed by exposure to hypoxia and can be negatively impacted by exposure to low, nonlethal DO concentrations (sublethal DO). We found that high sublethal area resulted in higher exposure and DO variability had a small effect on exposure. There was a large variation in exposure among individuals, which when combined with spatial variability of DO, can result in an underestimation of exposure when averaged.
Svenja Reents, Peter Mueller, Hao Tang, Kai Jensen, and Stefanie Nolte
Biogeosciences, 18, 403–411,Short summary
By conducting a flooding experiment with two genotypes of the salt-marsh grass Elymus athericus, we show considerable differences in biomass response to flooding within the same species. As biomass production plays a major role in sedimentation processes and thereby salt-marsh accretion, we emphasise the importance of taking intraspecific differences into account when evaluating ecosystem resilience to accelerated sea level rise.
Cara Nissen and Meike Vogt
Biogeosciences, 18, 251–283,Short summary
Using a regional Southern Ocean ecosystem model, we find that the relative importance of Phaeocystis and diatoms at high latitudes is controlled by iron and temperature variability, with light levels controlling the seasonal succession in coastal areas. Yet, biomass losses via aggregation and grazing matter as well. We show that the seasonal succession of Phaeocystis and diatoms impacts the seasonality of carbon export fluxes with ramifications for nutrient cycling and food web dynamics.
Jiangtao Li, Lingyuan Gu, Shijie Bai, Jie Wang, Lei Su, Bingbing Wei, Li Zhang, and Jiasong Fang
Biogeosciences, 18, 113–133,Short summary
Few studies have focused on the particle-attached (PA) and free-living (FL) microbes of the deep ocean. Here we determined PA and FL microbial communities along depth profiles of the SCS. PA and FL fractions accommodated divergent microbial compositions, and most of them are potentially generalists with PA and FL dual lifestyles. A potential vertical connectivity between surface-specific microbes and those in the deep ocean was indicated, likely through microbial attachment to sinking particles.
Saskia Brix, Karen J. Osborn, Stefanie Kaiser, Sarit B. Truskey, Sarah M. Schnurr, Nils Brenke, Marina Malyutina, and Pedro Martinez Arbizu
Biogeosciences, 17, 6163–6184,Short summary
The Clarion–Clipperton Fracture Zone (CCZ) located in the Pacific is commercially the most important area of proposed manganese nodule mining. Extraction of this will influence the life and distribution of small deep-sea invertebrates like peracarid crustaceans, of which >90 % are undescribed species new to science. We are doing a species delimitation approach as baseline for an ecological interpretation of species distribution and discuss the results in light of future deep-sea conservation.
Amal Jayakumar and Bess B. Ward
Biogeosciences, 17, 5953–5966,Short summary
Diversity and community composition of nitrogen-fixing microbes in the three main oxygen minimum zones of the world ocean were investigated using nifH clone libraries. Representatives of three main clusters of nifH genes were detected. Sequences were most diverse in the surface waters. The most abundant OTUs were affiliated with Alpha- and Gammaproteobacteria. The sequences were biogeographically distinct and the dominance of a few OTUs was commonly observed in OMZs in this (and other) studies.
Guillermo Feliú, Marc Pagano, Pamela Hidalgo, and François Carlotti
Biogeosciences, 17, 5417–5441,Short summary
The impact of Saharan dust deposition events on the Mediterranean Sea ecosystem was studied during a basin-scale survey (PEACETIME cruise, May–June 2017). Short-term responses of the zooplankton community were observed after episodic dust deposition events, highlighting the impact of these events on productivity up to the zooplankton level in the poorly fertilized pelagic ecosystems of the southern Mediterranean Sea.
Phillip Williamson, Hans-Otto Pörtner, Steve Widdicombe, and Jean-Pierre Gattuso
Revised manuscript accepted for BGShort summary
The reliability of ocean acidification research was challenged in early 2020 when a high-profile paper failed to corroborate previously-observed impacts of high CO2 on the behaviour of coral reef fish. We now know the reason why: the
replicatedstudies differed in many ways. Open-minded and collaborative assessment of all research results, both negative and positive, remains the best way to develop process-based understanding of the impacts of ocean acidification on marine organisms.
Katharine T. Bigham, Ashley A. Rowden, Daniel Leduc, and David A. Bowden
Revised manuscript accepted for BG
Douglas Lessa, Raphaël Morard, Lukas Jonkers, Igor M. Venancio, Runa Reuter, Adrian Baumeister, Ana Luiza Albuquerque, and Michal Kucera
Biogeosciences, 17, 4313–4342,Short summary
We observed that living planktonic foraminifera had distinct vertically distributed communities across the Subtropical South Atlantic. In addition, a hierarchic alternation of environmental parameters was measured to control the distribution of planktonic foraminifer's species depending on the water depth. This implies that not only temperature but also productivity and subsurface processes are signed in fossil assemblages, which could be used to perform paleoceanographic reconstructions.
Karl M. Attard and Ronnie N. Glud
Biogeosciences, 17, 4343–4353,Short summary
Light-use efficiency defines the ability of primary producers to convert sunlight energy to primary production. This report provides a framework to compute hourly and daily light-use efficiency using underwater eddy covariance, a recent technological development that produces habitat-scale rates of primary production for many different habitat types. The approach, tested on measured flux data, provides a useful means to compare habitat productivity across time and space.
Michael Lintner, Bianca Lintner, Wolfgang Wanek, Nina Keul, and Petra Heinz
Revised manuscript accepted for BG
Stacy Deppeler, Kai G. Schulz, Alyce Hancock, Penelope Pascoe, John McKinlay, and Andrew Davidson
Biogeosciences, 17, 4153–4171,Short summary
Our study showed how ocean acidification can exert both direct and indirect influences on the interactions among trophic levels within the microbial loop. Microbial grazer abundance was reduced at CO2 concentrations at and above 634 µatm, while microbial communities increased in abundance, likely due to a reduction in being grazed. Such changes in predator–prey interactions with ocean acidification could have significant effects on the food web and biogeochemistry in the Southern Ocean.
Mirjana Najdek, Marino Korlević, Paolo Paliaga, Marsej Markovski, Ingrid Ivančić, Ljiljana Iveša, Igor Felja, and Gerhard J. Herndl
Biogeosciences, 17, 3299–3315,Short summary
The response of Cymodocea nodosa to environmental changes was reported during a 15-month period. The meadow decline was triggered in spring by the simultaneous reduction of available light in the water column and the creation of anoxic conditions in the rooted area. This disturbance was critical for the plant since it took place during its recruitment phase when metabolic needs are maximal and stored reserves minimal. The loss of such habitat-forming seagrass is a major environmental concern.
Timm Schoening, Autun Purser, Daniel Langenkämper, Inken Suck, James Taylor, Daphne Cuvelier, Lidia Lins, Erik Simon-Lledó, Yann Marcon, Daniel O. B. Jones, Tim Nattkemper, Kevin Köser, Martin Zurowietz, Jens Greinert, and Jose Gomes-Pereira
Biogeosciences, 17, 3115–3133,Short summary
Seafloor imaging is widely used in marine science and industry to explore and monitor areas of interest. The selection of the most appropriate imaging gear and deployment strategy depends on the target application. This paper compares imaging platforms like autonomous vehicles or towed camera frames and different deployment strategies of those in assessing the megafauna abundance of polymetallic-nodule fields. The deep-sea mining industry needs that information for robust impact monitoring.
Tatsuro Tanioka and Katsumi Matsumoto
Biogeosciences, 17, 2939–2954,Short summary
We conducted an extensive literature survey (meta-analysis) on how the C : N : P ratio varies with change in key environmental drivers. We found that the expected reduction in nutrients and warming under the future climate change scenario is likely to result in increased C : P and C : N of marine phytoplankton. Further, our findings highlight the greater stoichiometric plasticity of eukaryotes over prokaryotes, which provide us insights on how to understand and model plankton.
Vanessa Joglar, Antero Prieto, Esther Barber-Lluch, Marta Hernández-Ruiz, Emilio Fernández, and Eva Teira
Biogeosciences, 17, 2807–2823,Short summary
Coastal marine ecosystems are among the most ecologically and economically productive areas providing a large fraction of ecosystem goods and services to human populations, and B vitamins have long been considered important growth factors for phytoplankton. Our findings indicate that the responses of microbial plankton to B-vitamin supply are mainly driven by the bacterial community composition and that microbial plankton in this area seems to be well adapted to cope with B-vitamin shortage.
Tasnim Patel, Henri Robert, Cedric D'Udekem D'Acoz, Koen Martens, Ilse De Mesel, Steven Degraer, and Isa Schön
Biogeosciences, 17, 2731–2744,Short summary
Exploitation of deep-sea resources in one of the largest ecosystems on the planet has rendered research of its biodiversity more urgent than ever before. We investigated the known habitats and connectivity of deep-sea scavenging amphipods and obtained important knowledge about several species. We also demonstrated that a long-term disturbance experiment has possibly reduced amphipod biodiversity. These data and further sampling expeditions are instrumental for formulating sustainable policies.
Daphne Cuvelier, Pedro A. Ribeiro, Sofia P. Ramalho, Daniel Kersken, Pedro Martinez Arbizu, and Ana Colaço
Biogeosciences, 17, 2657–2680,Short summary
Polymetallic nodule mining will remove hard substrata from the abyssal deep-sea floor. The only neighbouring ecosystems featuring hard substratum are seamounts, and their inhabiting fauna could aid in recovery post-mining. Nevertheless, first observations of seamount megafauna were very different from nodule-associated megafauna and showed little overlap. The possible uniqueness of these ecosystems implies that they should be included in management plans for the conservation of biodiversity.
Karen F. Wishner, Brad Seibel, and Dawn Outram
Biogeosciences, 17, 2315–2339,Short summary
Increasing deoxygenation and oxygen minimum zone expansion are consequences of global warming. Copepod species had different vertical distribution strategies and physiologies associated with oxygen profile variability (0–1000 m). Species (1) changed vertical distributions and maximum abundance depth, (2) shifted diapause depth, (3) changed diel vertical migration depths, or (4) changed epipelagic depth range in the aerobic mixed layer. Present-day variability helps predict future scenarios.
Magdalini Christodoulou, Timothy O'Hara, Andrew F. Hugall, Sahar Khodami, Clara F. Rodrigues, Ana Hilario, Annemiek Vink, and Pedro Martinez Arbizu
Biogeosciences, 17, 1845–1876,Short summary
Unexpectedly high diversity was revealed in areas licenced for polymetallic nodule mining exploration in the Pacific Ocean. For the first time, a comprehensive reference library including 287 novel ophiuroid sequences allocated to 43 species was produced. Differences in food availability along the nodule province of CCZ were reflected in the biodiversity patterns observed. The APEI3's dissimilarity with the exploration contract areas questions its ability to serve as a biodiversity reservoir.
Julie Meilland, Hélène Howa, Vivien Hulot, Isaline Demangel, Joëlle Salaün, and Thierry Garlan
Biogeosciences, 17, 1437–1450,Short summary
This study reports on planktonic foraminifera (PF) diversity and distribution in the Barents Sea. The species Globigerinita uvula and Turborotalita quinqueloba dominate the water column while surface sediments are dominated by Neogloboquadrina pachyderma. We hypothesize the unusual dominance of G. uvula in the water to be a seasonal signal or a result of climate forcing. Size-normalized-protein concentrations of PF show a northward decrease, suggesting biomass to vary with the environment.
Julien Richirt, Bettina Riedel, Aurélia Mouret, Magali Schweizer, Dewi Langlet, Dorina Seitaj, Filip J. R. Meysman, Caroline P. Slomp, and Frans J. Jorissen
Biogeosciences, 17, 1415–1435,Short summary
The paper presents the response of benthic foraminiferal communities to seasonal absence of oxygen coupled with the presence of hydrogen sulfide, considered very harmful for several living organisms. Our results suggest that the foraminiferal community mainly responds as a function of the duration of the adverse conditions. This knowledge is especially useful to better understand the ecology of benthic foraminifera but also in the context of palaeoceanographic interpretations.
Michele Casini, Martin Hansson, Alessandro Orio, and Karin Limburg
Revised manuscript accepted for BGShort summary
In the past twenty years the condition of the Eastern Baltic cod has dropped with large implications for the fishery. Our results show that during the same time, the cod population has moved deeper, while low-oxygenated waters detrimental for cod growth have shallowed. Cod has thus dwelled more in detrimental waters, which relates to the drop in its condition. This study, using long-term fish and hydrological monitoring data, evidences the impact of deoxygenation on fish biology and fishing.
Xiangqi Yi, Fei-Xue Fu, David A. Hutchins, and Kunshan Gao
Biogeosciences, 17, 1169–1180,Short summary
Combined effects of warming and light intensity were estimated in N2-fixing cyanobacterium Trichodesmium. Its physiological responses to warming were significantly modulated by light, with growth peaking at 27 °C under the light-saturating condition but being non-responsive across the range of 23–31 °C under the light-limiting condition. Light shortage also weakened the acclimation ability of Trichodesmium to warming, making light-limited Trichodesmium more sensitive to acute temperature change.
Jan Goleń, Jarosław Tyszka, Ulf Bickmeyer, and Jelle Bijma
Biogeosciences, 17, 995–1011,Short summary
We studied the organisation and dynamics of actin in foraminifera. Actin is one of the key structural proteins in most lifeforms. Our investigations show that in foraminifera it forms small granules, around 1 µm in diameter, that display rapid movement. This granularity is unusual in comparison to other organisms. We suppose that these granules are most likely involved in the formation of all types of pseudopods responsible for movement, food capturing, biomineralisation, and other functions.
Paulo Bonifácio, Pedro Martínez Arbizu, and Lénaïck Menot
Biogeosciences, 17, 865–886,Short summary
The patterns observed in the composition of polychaete assemblages were attributed to variations in food supply at the regional scale and nodule density at the local scale. The high levels of species replacement were mainly driven by rare species, leading to regional species pool estimates between 498 and 240 000 species. The high proportion of singletons seems reflect an under-sampling bias that is currently preventing the assessment of potential biodiversity loss due to nodule mining.
Stephanie Dutkiewicz, Pedro Cermeno, Oliver Jahn, Michael J. Follows, Anna E. Hickman, Darcy A. A. Taniguchi, and Ben A. Ward
Biogeosciences, 17, 609–634,Short summary
Phytoplankton are an essential component of the marine food web and earth's carbon cycle. We use observations, ecological theory and a unique trait-based ecosystem model to explain controls on patterns of marine phytoplankton biodiversity. We find that different dimensions of diversity (size classes, biogeochemical functional groups, thermal norms) are controlled by a disparate combination of mechanisms. This may explain why previous studies of phytoplankton diversity had conflicting results.
Emily White, Clara J. M. Hoppe, and Björn Rost
Biogeosciences, 17, 635–647,Short summary
The Arctic picoeukaryote Micromonas pusilla was acclimated to two pCO2 levels under a constant and a dynamic light, simulating more realistic light fields. M. pusilla was able to benefit from ocean acidification with an increase in growth rate, irrespective of the light regime. In dynamic light M. pusilla optimised its photophysiology for effective light usage during both low- and high-light periods. This highlights M. pusilla is likely to cope well with future conditions in the Arctic Ocean.
Oscar E. Romero, Karl-Heinz Baumann, Karin A. F. Zonneveld, Barbara Donner, Jens Hefter, Bambaye Hamady, Vera Pospelova, and Gerhard Fischer
Biogeosciences, 17, 187–214,Short summary
Monitoring of the multiannual evolution of populations representing different trophic levels allows for obtaining insights into the impact of climate variability in marine coastal upwelling ecosystems. By using a multiyear, continuous (1,900 d) sediment trap record, we assess the dynamics and fluxes of calcareous, organic and siliceous microorganisms off Mauritania (NW Africa). The experiment allowed for the recognition of a general sequence of seasonal variations of the main populations.
Ulrike Hanz, Claudia Wienberg, Dierk Hebbeln, Gerard Duineveld, Marc Lavaleye, Katriina Juva, Wolf-Christian Dullo, André Freiwald, Leonardo Tamborrino, Gert-Jan Reichart, Sascha Flögel, and Furu Mienis
Biogeosciences, 16, 4337–4356,Short summary
Along the Namibian and Angolan margins, low oxygen conditions do not meet environmental ranges for cold–water corals and hence are expected to be unsuitable habitats. Environmental conditions show that tidal movements deliver water with more oxygen and high–quality organic matter, suggesting that corals compensate unfavorable conditions with availability of food. With the expected expansion of oxygen minimum zones in the future, this study provides an example how ecosystems cope with extremes.
Alexia Dubuc, Ronald Baker, Cyril Marchand, Nathan J. Waltham, and Marcus Sheaves
Biogeosciences, 16, 3959–3976,Short summary
Little is known about how hypoxia influences mangrove fish assemblages. In situ video observations reveal species-specific avoidance strategies in response to developing hypoxia in a mangrove forest. Taxa commonly using mangroves could withstand hypoxia, while others usually associated with reef habitats were not recorded below 70 % saturation. These results suggest that hypoxia is an important factor shaping mangrove fish assemblages and could explain the low species richness usually observed.
Mariem Saavedra-Pellitero, Karl-Heinz Baumann, Miguel Ángel Fuertes, Hartmut Schulz, Yann Marcon, Nele Manon Vollmar, José-Abel Flores, and Frank Lamy
Biogeosciences, 16, 3679–3702,Short summary
Open ocean phytoplankton include coccolithophore algae, a key element in carbon cycle regulation with important feedbacks to the climate system. We document latitudinal variability in both coccolithophore assemblage and the mass variation in one particular species, Emiliania huxleyi, for a transect across the Drake Passage (in the Southern Ocean). Coccolithophore abundance, diversity and maximum depth habitat decrease southwards, coinciding with changes in the predominant E. huxleyi morphotypes.
Freija Hauquier, Lara Macheriotou, Tania N. Bezerra, Great Egho, Pedro Martínez Arbizu, and Ann Vanreusel
Biogeosciences, 16, 3475–3489,Short summary
Future mining operations in the deep sea provide a source of scientific uncertainty and call for detailed study of the ecosystem. We investigated one of the most diverse and abundant taxa present in deep-sea sediments, nematodes, and demonstrate the importance of sediment attributes for their communities. Especially species that are less common and have a limited spatial distribution will be vulnerable to mining-induced changes. Our findings can serve as a reference for future impact studies.
Haruka Takagi, Katsunori Kimoto, Tetsuichi Fujiki, Hiroaki Saito, Christiane Schmidt, Michal Kucera, and Kazuyoshi Moriya
Biogeosciences, 16, 3377–3396,Short summary
Photosymbiosis (endosymbiosis with algae) is an evolutionary important ecology for many marine organisms but has poorly been identified among planktonic foraminifera. In this study, we identified and characterized photosymbiosis of various species of planktonic foraminifera by focusing on their photosynthesis–related features. We finally proposed a new framework showing a potential strength of photosymbiosis, which will serve as a basis for future ecological studies of planktonic foraminifera.
Elina A. Virtanen, Alf Norkko, Antonia Nyström Sandman, and Markku Viitasalo
Biogeosciences, 16, 3183–3195,Short summary
Our understanding of the drivers of hypoxia fundamentally hinges on patterns of water circulation and vertical mixing that can be difficult to resolve in coastal regions. We identified areas prone to oxygen loss in a complex marine area without knowledge of biogeochemical properties, using only parameters which describe the enclosed seafloors with restricted water exchange. Our approach could help nutrient abatement measures and pinpoint areas where management actions are most urgently needed.
Jeffrey C. Drazen, Astrid B. Leitner, Sage Morningstar, Yann Marcon, Jens Greinert, and Autun Purser
Biogeosciences, 16, 3133–3146,Short summary
We investigated the fish and scavenger community after a deep seafloor disturbance experiment intended to simulate the effects of deep-sea mining. Fish density returned to background levels after several years; however the dominant fish was rarely found in ploughed habitat after 26 years. Given the significantly larger scale of industrial mining, these results could translate to population-level effects. The abyssal fish community at the site was similar to that in the Clarion–Clipperton Zone.
Scarlett Trimborn, Silke Thoms, Pascal Karitter, and Kai Bischof
Biogeosciences, 16, 2997–3008,Short summary
Ecophysiological studies on Antarctic cryptophytes to assess whether climatic changes such as ocean acidification and enhanced stratification affect their growth in Antarctic coastal waters in the future are lacking so far. Our results reveal beneficial effects of ocean acidification in conjunction with enhanced irradiance on growth and photosynthesis of the Antarctic cyrptophyte Geminigera cryophila. Hence, cryptophytes such as G. cryophila may be potential winners of these climatic changes.
Daffne C. López-Sandoval, Katherine Rowe, Paloma Carillo-de-Albonoz, Carlos M. Duarte, and Susana Agustí
Biogeosciences, 16, 2983–2995,Short summary
We addressed how the intertwined effect of temperature and nutrients modulates the metabolic response of planktonic communities in the Red Sea, one of the warmest seas on earth. Our study unveiled that photosynthesis increases at a faster pace than respiration rates for this group of organisms formed by microalgae, bacteria, and drifting animals. This anomaly is likely due to the nature of the basin where the warmest waters are frequently enriched with nutrients, which favours microalgae growth.
Camilla Parzanini, Christopher C. Parrish, Jean-François Hamel, and Annie Mercier
Biogeosciences, 16, 2837–2856,Short summary
This review synthesized current knowledge of deep-sea food webs and provided a preliminary analysis of global geographic patterns in the biochemical composition of deep-water organisms. Our results revealed both latitudinal and depth wise trends in the biochemical composition of deep-sea animals. In addition, the link across latitudes between surface primary production and deep-water communities was highlighted, which has important implications in the face of global climate change.
Susann Rossbach, Vincent Saderne, Andrea Anton, and Carlos M. Duarte
Biogeosciences, 16, 2635–2650,Short summary
Giant clams including the species Tridacna maxima are unique among bivalves as they live in symbiosis with unicellular algae and generally function as net photoautotrophs. Light is therefore crucial for these species to thrive. We show that net calcification and photosynthetic rates of T. maxima are light dependent, with maximum rates at conditions comparable to 4 m water depth, reflected also in the depth-related distribution in the Red Sea with maximum abundances in shallow sunlit coral reefs.
Lisa Mevenkamp, Katja Guilini, Antje Boetius, Johan De Grave, Brecht Laforce, Dimitri Vandenberghe, Laszlo Vincze, and Ann Vanreusel
Biogeosciences, 16, 2329–2341,Short summary
To elucidate the potential effects of crushed nodule particle deposition on abyssal meiobenthos, we covered abyssal soft sediment in the Peru Basin (4200 m depth) with approximately 2 cm of this nodule material for 11 d. About half of the meiobenthos migrated from the sediment into the added material, and nematode feeding type proportions in that added layer were altered. These results considerably contribute to our understanding of the short-term responses of deep-sea meiobenthos to burial.
Maria Grigoratou, Fanny M. Monteiro, Daniela N. Schmidt, Jamie D. Wilson, Ben A. Ward, and Andy Ridgwell
Biogeosciences, 16, 1469–1492,Short summary
The paper presents a novel study based on the traits of shell size, calcification and feeding behaviour of two planktonic foraminifera life stages using modelling simulations. With the model, we tested the cost and benefit of calcification and explored how the interactions of planktonic foraminifera among other plankton groups influence their biomass under different environmental conditions. Our results provide new insights into environmental controls in planktonic foraminifera ecology.
Shanying Tong, David A. Hutchins, and Kunshan Gao
Biogeosciences, 16, 561–572,Short summary
Most previous studies concerning the effects of environmental changes on marine organisms have been carried out under
photosynthetically active radiation onlyconditions, with solar ultraviolet radiation (UVR) not being considered. In this study, we found that UVR can counteract the negative effects of the
greenhousetreatment on the calcification rate to photosynthesis rate ratio, and may be a key stressor when considering the impacts of future greenhouse conditions on E. huxleyi.
Catherine A. Pfister and Mark A. Altabet
Biogeosciences, 16, 193–206,Short summary
Microbial assemblages on host plants and animals are an increasingly recognized biological phenomenon. We present evidence that microbes in association with mussels and seaweeds are contributing greatly to nitrogen cycling in coastal marine areas, often many times that of the microbes that are simply free-living in seawater. The addition of dissolved organic carbon increased nutrient uptake by microbes, suggesting that coastal species enhance microbial metabolism through resource provisioning.
François Carlotti, Marc Pagano, Loïc Guilloux, Katty Donoso, Valentina Valdés, Olivier Grosso, and Brian P. V. Hunt
Biogeosciences, 15, 7273–7297,Short summary
The paper characterizes the zooplankton community and plankton food web processes between New Caledonia and Tahiti (tropical South Pacific) during the austral summer 2015. In this region, the pelagic production depends on N2 fixation by diazotroph microorganisms on which the zooplankton community feeds, supporting a pelagic food chain ending with valuable tuna fisheries. We estimated a contribution of up to 75 % of diazotroph‐derived nitrogen to zooplankton biomass in the Melanesian archipelago.
Ana Martinez, Laura Hernández-Terrones, Mario Rebolledo-Vieyra, and Adina Paytan
Biogeosciences, 15, 6819–6832,Short summary
Our study at low-pH submarine springs suggests that ocean acidification may reduce the number of Caribbean benthic foraminifera, particularly those species that form carbonate shells. This may have subsequent repercussions on the global carbon cycle and marine food webs that depend on benthic foraminifera.
Janet E. Burke, Willem Renema, Michael J. Henehan, Leanne E. Elder, Catherine V. Davis, Amy E. Maas, Gavin L. Foster, Ralf Schiebel, and Pincelli M. Hull
Biogeosciences, 15, 6607–6619,Short summary
Metabolic rates are sensitive to environmental conditions and can skew geochemical measurements. However, there is no way to track these rates through time. Here we investigate the controls of test porosity in planktonic foraminifera (organisms commonly used in paleoclimate studies) as a potential proxy for metabolic rate. We found that the porosity varies with body size and temperature, two key controls on metabolic rate, and that it can respond to rapid changes in ambient temperature.
Anna Roik, Till Röthig, Claudia Pogoreutz, Vincent Saderne, and Christian R. Voolstra
Biogeosciences, 15, 6277–6296,Short summary
In this study we collected in situ accretion/erosion rates and abiotic/biotic variables to estimate carbonate budgets and ecological drivers of coral reef growth in the central Red Sea. Our data suggest that reef growth is comparable to estimates of other regions, but the erosive forces in the Red Sea are not as pronounced. Comparison with recent data suggests that Red Sea reef growth might not have decreased over the past decades, despite warming, calling for more detailed investigations.
Craig S. Young and Christopher J. Gobler
Biogeosciences, 15, 6167–6183,Short summary
Photosynthetic activity and/or nitrate assimilation by the macroalgae Ulva buffered carbonate chemistry and yielded enhanced growth of bivalves by mitigating the harmful effects of elevated CO2 levels. This benefit was not limited to acidified conditions, as evidenced by increased bivalve growth in the presence of Ulva within ambient CO2 treatments. The ability of macroalgae to buffer carbonate chemistry may be increasingly important for calcifying organisms vulnerable to ocean acidification.
Anand, P., Elderfield, H., and Conte, M. H.: Calibration of Mg ∕ Ca thermometry in planktonic foraminifera from a sediment trap time series, Paleoceanography, 18, 1050 https://doi.org/10.1029/2002PA000846, 2003.
Aldridge, D., Beer, C. J., and Purdie, D. A.: Calcification in the planktonic foraminifera Globigerina bulloides linked to phosphate concentrations in surface waters of the North Atlantic Ocean, Biogeosciences, 9, 1725–1739, https://doi.org/10.5194/bg-9-1725-2012, 2012.
Allers, E., Wright, J. J., Konwar, K. M., Howes, C. G., Beneze, E., Hallam, S. J., and Sullivan, M. B.: Diversity and population structure of Marine Group A bacteria in the Northeast subarctic Pacific Ocean, ISME J., 7, 256–268, https://doi.org/10.1038/ismej.2012.108, 2012.
André, A., Quillévéré, F., Morard, R., Ujiié, Y., Escarguel, G., de Vargas, C., de Garidel-Thoron, T., and Douady, C. J.: SSU rDNA Divergence in Planktonic Foraminifera: Molecular Taxonomy and Biogeographic Implications, Plos One, 9, e104641, https://doi.org/10.1371/journal.pone.0104641, 2014.
Ashton, M., Rosado, W., Govind, N. S., and Tosteson, T. R.: Culturable and nonculturable bacterial symbionts in the toxic benthic dinoflagellate Ostreopsis lenticularis, Toxicon, 42, 419–424, https://doi.org/10.1016/S0041-0101(03)00174-0, 2003.
Apprill, A., McNally, S., Parsons, R., and Weber, L.: Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton, Aquat. Microb. Ecol., 75, 129–137, https://doi.org/10.3354/ame01753, 2015.
Bé, A. W. H., Spero, H. J., and Anderson, O. R.: Effects of symbiont elimination and reinfection on the life processes of the planktonic foraminifer Globigerinoides sacculifer, Mar. Biol., 70, 73–86, https://doi.org/10.1007/BF00397298, 1982.
Beier, C. L., Horn, M., Michel, R., Schweikert, M., Görtz, H.-D., and Wagner, M.: The genus Caedibacter comprises endosymbionts of Paramecium spp. related to the Rickettsiales (Alphaproteobacteria) and to Francisella tularensis (Gammaproteobacteria), Appl. Environ. Microb., 68, 6043–6050, https://doi.org/10.1128/AEM.68.12.6043-6050.2002, 2002.
Bemis, B. E., Spero, H. J., Bijma, J., and Lea, D. W.: Reevaluation of the oxygen isotopic composition of planktonic foraminifera: Experimental results and revised paleotemperature equations, Paleoceanography, 13, 150–160, https://doi.org/10.1029/98PA00070, 1998.
Bemis, B. E., Spero, H. J., Lea, D. W., and Bijma, J.: Temperature influence on the carbon isotopic composition of Globigerina bulloides and Orbulina universa (planktonic foraminifera), Mar. Micropaleontol., 38, 213–228, https://doi.org/10.1016/S0377-8398(00)00006-2, 2000.
Bemis, B. E., Spero, H. J., and Thunell, R. C.: Using species-specific paleotemperature equations with foraminifera: a case study in the Southern California Bight, Mar. Micropaleontol., 46, 405–430, https://doi.org/10.1016/S0377-8398(02)00083-X, 2002.
Bernhard, J. M., Buck, K. R., Farmer, M. A., and Bowser, S. S.: The Santa Barbara Basin is a symbiosis oasis, Nature, 403, 77–80, https://doi.org/10.1038/47476, 2000.
Bernhard, J., Habura, A., and Bowser, S.: An endobiont-bearing allogromiid from the Santa Barbara Basin: Implications for the early diversification of foraminifera, J. Geophys. Res., 111, G03002, https://doi.org/10.1029/2005JG000158, 2006.
Bernhard, J. M., Edgcomb, V. P., Casciotti, K. L., McIlvin, M. R., and Beaudoin, D. J.: Denitrification likely catalyzed by endobionts in an allogromiid foraminifer, ISME J., 6, 951–960, https://doi.org/10.1038/ismej.2011.171, 2012.
Bidigare R. R., Schofield, O., and Prézelin, B. B.: Influence of zeaxanthin on quantum yield of photosynthesis of Synechococcus clone WH7803 (DC2), Mar. Ecol. Prog. Ser., 56, 177–188, https://doi.org/10.3354/meps056177, 1989.
Bijma, J., Erez, J., and Hemleben, C.: Lunar and semi-lunar reproductive cycles in some spinose planktonic foraminifers, J. Formin. Res., 20, 117–127, https://doi.org/10.2113/gsjfr.20.2.117, 1990.
Bijma, J., Hemleben, C., Huber, B. T., Erlenkeuser, H., and Kroon, D.: Experimental determination of the ontogenetic stable isotope variability in two morphotypes of Globigerinella siphonifera (d'Orbigny), Mar. Micropaleontol., 35, 141–160, 1998.
Bijma, J., Spero, H. J., and Lea, D. W.: Reassessing foraminiferal stable isotope geochemistry: Impact of the oceanic carbonate system (experimental results), in: Use of proxies in paleoceanography, edited by: Fischer, G. and Wefer, G., Springer-Verlag, Berlin Heidelberg New York, 489–512, 1999.
Bird, C., Darling, K. F., Russell, A. D., Davis, C. V., Fehrenbacher, J., Free, A., Wyman, M., and Ngwenya, B. T.: Sequencing Read Archive data set, BioProject accession number PRJNA341960, Cyanobacterial endobionts wihtin a major marine planktonic calcifier (Globigerina bulloides, foraminifera) revealed by 16S rRNA metabarcoding, available at: http://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA341960, last access: 23 February 2017.
Bright, M. and Bulgheresi, S.: A complex journey: transmission of microbial symbionts, Nat. Rev. Microbiol., 8, 218–230, https://doi.org/10.1038/nrmicro2262, 2010.
Buck, K. R. and Bentham, W. N.: A novel symbiosis between a cyanobacterium, Synechococcus sp., an aplastidic protist, Solenicola setigera, and a diatom, Leptocylindrus mediterraneus, in the open ocean, Mar. Biol., 132, 349–355, https://doi.org/10.1007/s002270050401, 1998.
Buck, K. R. and Bernhard, J. M.: Protistan-Prokaryotic symbioses in deep-sea sulfidic sediments, in: Symbiosis: mechanisms and model systems, edited by: Seckbach, J., Kluwer Academic Publishers, https://doi.org/10.1007/0-306-48173-1, 2006.
Campbell, L. and Carpenter E. J.: Diel patterns of cell division in marine Synechococcus spp. (Cyanobacteria): use of the frequency of dividing cells technique to measure growth rate, Mar. Ecol. Prog. Ser., 32, 139–148, 1986
Caporaso, G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F., Costello, E., Fierer, N., Peña, A., Goodrich, J., Gordon, J., Huttley, G., Kelley, S., Knights, D., Koenig, J., Ley, R., Lozupone, C., McDonald, D., Muegge, B., Pirrung, M., Reeder, J., Sevinsky, J., Turnbaugh, P., Walters, W., Widmann, J., Yatsunenko, T., Zaneveld, J., and Knight, R.: QIIME allows analysis of high-throughput community sequencing data, Nat. Methods, 7, 335–336, https://doi.org/10.1038/nmeth.f.303, 2010.
Caporaso, G., Lauber, C., Walters, W., Berg-Lyons, D., Huntley, J., Fierer, N., Owens, S., Betley, J., Fraser, L., Bauer, M., Gormley, N., Gilbert, J., Smith, G., and Knight, R.: Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms, ISME J., 6, 1621–1624, https://doi.org/10.1038/ismej.2012.8, 2012.
Caron, D. A., Michaels, A. F., and Swanberg, N. R.: Primary productivity by symbiont-bearing planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda, J. Plankton Res., 17, 103–129, https://doi.org/10.1093/plankt/17.1.103, 1995.
Cavalier-Smith, T. and Chao, E. E.: Phylogeny and classification of phylum Cercozoa (Protozoa), Protist, 154, 341–58, https://doi.org/10.1078/143446103322454112, 2003.
Checkley, D. M. and Barth, J. A.: Patterns and processes in the California Current System, Prog. Oceanogr., 83, 49–64, https://doi.org/10.1016/j.pocean.2009.07.028, 2009.
Chow, C.-E. T., Sachdeva, R., Cram, J. A., Steele, J. A., Needham, D. M., Patel, A., Parada, A. E., and Fuhrman, J. A.: Temporal variability and coherence of euphotic zone bacterial communities over a decade in the Southern California Bight, ISME J., 7, 2259–2273, https://doi.org/10.1038/ismej.2013.122, 2013
Cram, J. A., Chow, C.-E. T., Sachdeva, R., Needham, D. M., Parada, A. E., Steele, J. A., and Fuhrman, J. A.: Seasonal and interannual variability of the marine bacterioplankton community throughout the water column over ten years, ISME J., 9, 563–580, https://doi.org/10.1038/ismej.2014.153, 2015.
Curry, W. B. and Matthews, R. K.: Equilibrium 18O fractionation in small size fraction planktic foraminifera: Evidence from recent Indian Ocean sediments, Mar. Micropaleontol., 6, 327–337, 1981.
Darling, K. F., Wade, C. M., Kroon, D., Leigh Brown, A. J., and Bijma, J.: The diversity and distribution of modern planktic foraminiferal small subunit ribosomal RNA genotypes and their potential as tracers of present and past ocean circulations, Paleoceanography, 14, 3–12 https://doi.org/10.1029/1998PA900002, 1999.
Darling, K. F., Wade, C. M., Stewart, I. A., Kroon, D., Dingle, R., and Brown, A. J.: Molecular evidence for genetic mixing of Arctic and Antarctic subpolar populations of planktonic foraminifers, Nature, 405, 43–47, https://doi.org/10.1038/35011002, 2000.
Darling, K. F., Kucera, M., Wade, C. M., von Langen, P., and Pak, D.: Seasonal distribution of genetic types of planktonic foraminifer morphospecies in the Santa Barbara Channel and its paleoceanographic implications, Paleoceanography, 18, 1032–1043, https://doi.org/10.1029/2001PA000723, 2003.
Darling, K. F. and Wade, C.: The genetic diversity of planktic foraminifera and the global distribution of ribosomal RNA genotypes, Mar. Micropaleontol., 67, 216–238, https://doi.org/10.1016/j.marmicro.2008.01.009, 2008.
Davis, C. V., Hill, T. M., Russell, A. D., Gaylord, B. P., and Jahncke, J. and: Seasonality in planktic foraminifera of the central California coastal upwelling region, Biogeosciences, 13, 5139–5150, https://doi.org/10.5194/bg-13-5139-2016, 2016
Decelle, J., Colin, S., and Foster, R. A.: Photosymbiosis in marine planktonic protists, in: Marine Protists: Diversity and Dynamics, edited by: Ohtsuka, S., Suzaki, T., Horiguchi, T., Suzuki, N. and Not, F., Springer Japan, https://doi.org/10.1007/978-4-431-55130-0_19, 2015.
DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., Huber, T., Dalevi, D., Hu, P., and Andersen, G. L.: Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB, Appl. Environ. Microb., 72, 5069–5072, https://doi.org/10.1128/AEM.03006-05, 2006.
Deuser, W. G., Ross, E. H., Hemleben, C., and Spindler, M.: Seasonal changes in species composition, numbers, mass, size, and isotopic composition of planktonic foraminifera settling into the deep Sargasso Sea, Palaeogeogr., Palaeocl., 33, 103–127, https://doi.org/10.1016/0031-0182(81)90034-1, 1981.
de Vargas, C., Renaud, S., Hilbrecht, H., and Pawlowski, J.: Pleistocene adaptive radiation in Globorotalia truncatulinoides: genetic, morphologic, and environmental evidence, Paleobiology, 27, 104–125, https://doi.org/10.1666/0094-8373(2001)027<0104:PARIGT>2.0.CO;2, 2001.
Edgar, R., Haas, B. J., Clemente, J. C., Quince, C., and Knight, R.: UCHIME improves sensitivity and speed of chimera detection, Bioinformatics, 27, 2194–2200, https://doi.org/10.1093/bioinformatics/btr381, 2011.
Eggins, S. M., Sadekov, A., and De Deckker, P.: Modulation and daily banding of Mg/Ca in Orbulina universa tests by symbiont photosynthesis and respiration: a complication for seawater thermometry?, Earth Planet. Sc. Lett., 225, 411–419, https://doi.org/10.1016/j.epsl.2004.06.019, 2004.
Febvre-Chevalier, C.: Constitution ultrastructural de Globigerina bulloides d' Orbigny (Rhizopoda-Foraminifera), Protistologica, 7, 311–324, 1971.
Feely, R. A., Sabine, C. L., Lee, K., Berelson, W., Kleypas, J., Fabry, V. J., and Millero, F. J.: Impact of anthropogenic CO2 on the CaCO3 system in the oceans, Science, 305, 362–6, https://doi.org/10.1126/science.1097329, 2004.
Field, D. B.: Variability in vertical distributions of planktonic foraminifera in the California Current: Relationships to vertical ocean structure, Paleoceanography, 19, PA2014, https://doi.org/10.1029/2003PA000970, 2004.
Fokin, S. I.: Bacterial endocytobionts of ciliophora and their interactions with the host cell, Int. Rev. Cytol., 236, 181–249, https://doi.org/10.1016/S0074-7696(04)36005-5, 2004.
Fraile, I., Schulz, M., Mulitza, S., and Kucera, M.: Predicting the global distribution of planktonic foraminifera using a dynamic ecosystem model, Biogeosciences, 5, 891–911, https://doi.org/10.5194/bg-5-891-2008, 2008.
Fuller, N. J., Marie, D., Partensky, F., Vaulot, D., Post, A. F., and Scanlan, D. J.: Clade-specific 16S ribosomal DNA oligonucleotides reveal the pre-dominance of a single marine Synechococcus clade throughout a stratified water column in the Red Sea, Appl. Environ. Microb., 69, 2430–2443, https://doi.org/10.1128/AEM.69.5.2430-2443.2003, 2003.
García-Reyes and Largier: Seasonality of coastal upwelling off central and northern California: New insights, including temporal and spatial variability, J. Geophys. Res.-Oceans, 117, C03028, https://doi.org/10.1029/2011jc007629, 2012.
Gast, R. J., Sanders, R. W., and Caron, D. A.: Ecological strategies of protists and their symbiotic relationships with prokaryotic microbes, Trends Microbiol., 17, 563–569, https://doi.org/10.1016/j.tim.2009.09.001, 2009.
Gastrich, M.: Ultrastructure of a new intracellular symbiotic alga found within planktonic foraminifera, J. Phycol., 23, 623–632, https://doi.org/10.1111/j.1529-8817.1987.tb04215.x, 1987.
Gastrich, M. and Bartha, R.: Primary productivity in the planktonic foraminifer Globigerinoides ruber (d'Orbigny), J. Foramin. Res., 18, 137–142, https://doi.org/10.2113/gsjfr.18.2.137, 1988.
Geslin, E., Risgaard-Petersen, N., Lombard, F., Metzger, E., Langlet, D., and Jorissen, F.: Oxygen respiration rates of benthic foraminifera as measured with oxygen microsensors, J. Exp. Mar. Biol. Ecol., 396, 108–114, https://doi.org/10.1016/j.jembe.2010.10.011, 2011.
Gilbert, J. A., Jansson, J. K., and Knight, R.: The Earth Microbiome Project: successes and aspirations, BMC Biol., 12, 69–72, https://doi.org/10.1186/s12915-014-0069-1, 2014.
Gilbert, S. F., Sapp, J., and Tauber, A. I.: A symbiotic view of life: we have never been individuals, Q. Rev. Biol., 87, 325–341 https://doi.org/10.1086/668166, 2012.
Giovannoni, S. J., Britschgi, T. B., Moyer, C. L., and Field, K. G.: Genetic diversity in Sargasso Sea bacterioplankton, Nature, 345, 60–63, https://doi.org/10.1038/345060a0, 1990.
Hannah, F., Rogerson, R., and laybourne-Parry, J.: Respiration rates and biovolumes of common benthic foraminifera (Protozoa), J. Mar. Biol. Assoc. UK, 74, 301–312, https://doi.org/10.1017/S0025315400039345, 1994.
Healy-Williams, N., Ehrlich, R., and Williams, D. F.: Morphometric and stable isotopic evidence for subpopulations of Globorotalia truncatulinoides, J. Foramin. Res., 15, 242–253, https://doi.org/10.2113/gsjfr.15.4.242, 1985.
Hemleben, C., Spindler, M., and Anderson, O. R.: Modern planktonic foraminifera, Springer-Verlag, New York, 1989
Henderson, G. M.: New oceanic proxies for paleoclimate, Earth Planet. Sc. Lett., 203, 1–13, https://doi.org/10.1016/S0012-821X(02)00809-9, 2002.
Holligan, P. M. and Robertson, J. E.: Significance of ocean carbonate budgets for the global carbon cycle, Glob. Change Biol., 2, 85–95, https://doi.org/10.1111/j.1365-2486.1996.tb00053.x, 1996.
Holzmann, M. and Pawlowski, J.: Preservation of foraminifera for DNA extraction and PCR amplification, J. Foramin. Res., 26, 264–267, https://doi.org/10.2113/gsjfr.26.3.264, 1996.
Hönisch, B., Bijma, J., Russell, A. D. and Spero, H. J, Palmer, M. R., Zeebe, R. E., and Eisenhauer, A.: The influence of symbiont photosynthesis on the boron isotopic composition of foraminifera shells, Mar. Micropaleontol., 49, 87–96, https://doi.org/10.1016/S0377-8398(03)00030-6, 2003.
Huber, B. T., Bijma, J., and Darling, K. F.: Cryptic speciation in the living planktonic foraminifer Globigerinella siphonifera (d'Orbigny), Paleobiology, 23, 33–62, https://doi.org/10.1017/S0094837300016638, 1997
Hugenholtz, P., Pitulle, C., Hershberger, K. L., and Pace, N. R.: Novel division level bacterial diversity in a Yellowstone hot spring, J. Bacteriol., 180, 366–376, 1998.
Iglesias-Rodriguez, M. D., Armstrong, R., Feely, R., Hood, R., Kleypas, J., Milliman, J. D., Sabine, C., and Sarmiento, J.: Progress made in study of ocean's calcium carbonate budget, Eos, Tran. Amer. Geophys. Un., 83, 365–375, https://doi.org/10.1029/2002eo000267, 2002.
Jacox, M., Fiechter, J., Moore, A., and Edwards, C.: ENSO and the California Current coastal upwelling response, J. Geophys. Res.-Oceans, 120, 1691–1702, https://doi.org/10.1002/2014jc010650, 2015.
Kahn, M. I. and Williams, D. F.: Oxygen and carbon isotopic composition of living planktonic foraminifera from the northeast Pacific Ocean, Palaeogeogr. Palaeocl., 33, 47–69, https://doi.org/10.1016/0031-0182(81)90032-8, 1981.
Katz, M. E., Cramer, B. S., Franzese, A., Hönisch, B., Miller, K. G., Rosenthal, Y., and Wright, J. D.: Traditional and emerging geochemical proxies in foraminifera, J. Foramin. Res., 40, 165–192, https://doi.org/10.2113/gsjfr.40.2.165, 2010.
Kleijne, A., Kroon, D., and Zevenboom, W.: Phytoplankton and foraminiferal frequencies in northern Indian Ocean and Red Sea surface waters, Neth. J. Sea Res., 24, 531–539, https://doi.org/10.1016/0077-7579(89)90131-2, 1989.
Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K., and Schloss, P. D.: Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform, Appl. Environ. Microb., 79, 5112–5120, https://doi.org/10.1128/AEM.01043-13, 2013.
Kroon, D. and Darling, K. F.: Size and upwelling control of the stable isotope composition of Neogloboquadrina dutertrei (d'Orbigny), Globigerinoides ruber (d'Orbigny) and Globigerina bulloides d'Orbigny: examples from the Panama Basin and Arabian Sea, J. Foramin. Res., 25, 39–52, https://doi.org/10.2113/gsjfr.25.1.39, 1995
Kucera, M. and Darling, K. F.: Cryptic species of planktonic foraminifera: their effect on palaeoceanographic reconstructions, Philos. T. Roy. Soc. A, 360, 695–718, https://doi.org/10.1098/rsta.2001.0962, 2002.
Kucera, M. and Kennett, J. P.: Causes and consequences of a middle Pleistocene origin of the modern planktonic foraminifer Neogloboquadrina pachyderma sinistral, Geology, 30, 539–542, https://doi.org/10.1130/0091-7613(2002)030<0539:CACOAM>2.0.CO;2, 2002.
Kucera, M.: Planktonic Foraminifera as Tracers of Past Oceanic Environments, in: Developments in Marine Geology, edited by: Hillaire-Marcel, C. and De Vernal, A., Elsevier, 1, 213–262, https://doi.org/10.1016/S1572-5480(07)01011-1, 2007.
Laurence, M., Hatzis, C., and Brash, D. E.: Common contaminants in next-generation sequencing that hinder discovery of low-abundance microbes, PLoS One, 9, e97876, https://doi.org/10.1371/journal.pone.0097876, 2014.
Lee, J. J., McEnery, M., Pierce, S., Freudenthal, H. D., and Muller, W. A.: Tracer Experiments in Feeding Littoral Foraminifera, J. Eukaryot. Microbiol., 13, 659–670, https://doi.org/10.1111/j.1550-7408.1966.tb01978.x, 1966.
Lombard, F., Erez, J., Michel, E., and Labeyrie, L.: Temperature effect on respiration and photosynthesis of the symbiont-bearing planktonic foraminifera Globigerinoides ruber, Orbulina universa, and Globigerinella siphonifera, Limnol. Oceanogr., 54, 210–218, https://doi.org/10.4319/lo.2009.54.1.0210, 2009.
Lombard, F., Labeyrie, L., Michel, E., Bopp, L., Cortijo, E., Retailleau, S., Howa, H., and Jorissen, F.: Modelling planktic foraminifer growth and distribution using an ecophysiological multi-species approach, Biogeosciences, 8, 853–873, https://doi.org/10.5194/bg-8-853-2011, 2011.
Manno, C, Morato, N., and Bellerby, R.: Effect of ocean acidification and temperature increase on the planktonic foraminifer Neogloboquadrina pachyderma (sinstral), Polar Biol., 35, 1311–1319, https://doi.org/10.1007/s00300-012-1174-7, 2012.
Martin, P., Dyhrman, S. T., Lomas, M. W., Poulton, N. J., and Van Mooy, B. A. S.: Accumulation and enhanced cycling of polyphosphate by Sargasso Sea plankton in response to low phosphorus, P. Natl. Acad. Sci. USA, 111, 8089–8094, https://doi.org/10.1073/pnas.1321719111, 2014.
Mashiotta, T. A., Lea, D. W., and Spero, H. J.: Experimental determination of cadmium uptake in shells of the planktonic foraminifera Orbulina universa and Globigerina bulloides: Implications for surface water paleoreconstructions, Geochim. Cosmochim. Ac., 61, 4053–4065, https://doi.org/10.1016/S0016-7037(97)00206-8, 1997.
Mitra, A., Flynn, K. J., Tillmann, U., Raven, J. A., Caron, D., Stoeker, D. K., Not, F., Hansen, P. J., Hallegraeff, G., Sanders, R., Wilken, S., MacManus, G., Johnson, M., Pitta, P., Våge, S., Berge, T., Calbet, A., Thingstad, F., Jin Jeong, H., Burkholder, J., Glibert, P. M., Granéli, E., and Lundgren, V.: Defining Planktonic Protist Functional Groups on Mechanisms for Energy and Nutrient Acquisition: Incorporation of Diverse Mixotrophic Strategies, Protist, 167, 106–120, https://doi.org/10.1016/l.protis.2016.01.003, 2016.
Morard, R., Quillévéré, F., Escarguel, G., de Garidel-Thoron, T., de Vargas, C., and Kucera, M.: Ecological modeling of the temperature dependence of cryptic species of planktonic Foraminifera in the Southern Hemisphere, Palaeogeogr. Palaeocl., 391, 13–33, https://doi.org/10.1016/l.palaeo.2013.05.011, 2013.
Morris, R. M, Rappé, M. S., Connon, S. A, Vergin, K. L., Siebold, W. A, Carlson, C. A., and Giovannoni, S. J.: SAR11 clade dominates ocean surface bacterioplankton communities, Nature, 420, 806–810, https://doi.org/10.1038/nature01240, 2002.
Mühling, M., Fuller, N. J., Millard, A., Somerfield, P. J., Marie, D., Wilson, W. H., Scanlan, D. J., Post, A. F., Joint, I., and Mann, N. H.: Genetic diversity of marine Synechococcus and co-occurring cyanophage communities: evidence for viral control of phytoplankton, Environ. Microbiol., 7, 499–508, https://doi.org/10.1111/j.1462-2920.2005.00713.x, 2005.
Murray, J.: On the distribution of the pelagic foraminifera at the surface and on the floor of the ocean, Nat. Sci., 11, 17–24, 1897.
Naidu, P. D. and Malmgren, B. A.: Relationship between late Quaternary upwelling history and coiling properties of Neogloboquadrina pachyderma and Globigerina bulloides in the Arabian Sea, J. Foramin. Res., 26, 64–70, https://doi.org/10.2113/gsjfr.26.1.64, 1996.
Nowack, E. C. M. and Melkonian, M.: Endosymbiotic associations within protists, Philos. T. Roy. Soc. B, 365, 699–712, https://doi.org/10.1098/rstb.2009.0188, 2010.
Nübel, U., Garcia-Pichel, F., and Muyzer, G.: PCR primers to amplify 16S rRNA genes from cyanobacteria, Appl. Environ. Microb., 63, 3327–32, 1997.
Orsi, W., Charvet, S., Vd'ačný, P., Bernhard, J. M., and Edgcomb, V. P: Prevalence of partnerships between bacteria and ciliates in oxygen-depleted marine water columns, Front. Microbiol., 3, 341, https://doi.org/10.3389/fmicb.2012.00341, 2012.
Paerl, R. W., Johnson, K. S., Welsh, R. M., Worden, A. Z., Chavez, F. P., and Zehr, J. P.: Differential Distributions of Synechococcus Subgroups Across the California Current System, Front. Microbiol., 2, 59–71, https://doi.org/10.3389/fmicb.2011.00059, 2011.
Padua, R. A., Parrado, A., Larghero, J., and Chomienne, C.: UV and clean air result in contamination-free PCR, Leukemia, 13, 1898–1899, 1999.
Pagaling, E., Strathdee, F., Spears, B. M., Cates, M. E., Allen, R. J., and Free, A.: Community history affects the predictability of microbial ecosystem development, ISME J., 8, 19–30, https://doi.org/10.1038/ismej.2013.150, 2014.
Paoli, A., Celussi, M., Del Negro, P. Umani, S. F., and Talarico, L.: Ecological advantages from light adaptation and heterotrophic-like behavior in Synechococcus harvested from the Gulf of Trieste (Northern Adriatic Sea), FEMS Microbiol. Ecol., 64, 153–327, https://doi.org/10.1111/j.1574-6941.2008.00459.x, 2008.
Parada, A., Needham, D., and Fuhrman, J.: Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples, Environ. Microbiol., 18, 1403–1414, https://doi.org/10.1111/1462-2920.13023, 2016.
Partensky, F., Blanchot, J., and Vaulot, D.: Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review, Bulletin de l'Institut océanographique, available at: http://horizon.documentation.ird.fr/exl-doc/pleins_textes/divers15-02/010019788.pdf (last access: 22 February 2017), 1999.
Rappé, M. S. and Giovannoni, S. J: The uncultured microbial majority, Annu. Rev. Microbiol., 57, 369–394, https://doi.org/10.1146/annurev.micro.57.030502.090759, 2003.
Richardson, T. L. and Jackson, G. A.: Small phytoplankton and carbon export from the surface ocean, Science, 315, 838–40, https://doi.org/10.1126/science.1133471, 2007.
Ridgwell, A. and Zeebe, R. E.: The role of the global carbonate cycle in the regulation and evolution of the Earth system, Earth Planet. Sc. Lett., 234, 299–315, https://doi.org/10.1016/j.epsl.2005.03.006, 2005.
Rink, S., Kühl, M., Bijma, J., and Spero, H. J.: Microsensor studies of photosynthesis and respiration in the symbiotic foraminifer Orbulina universa, Mar. Biol., 131, 583–595, https://doi.org/10.1007/S002270050350, 1998.
Roy, T., Lombard, F., Bopp, L., and Gehlen, M.: Projected impacts of climate change and ocean acidification on the global biogeography of planktonic Foraminifera, Biogeosciences, 12, 2873–2889, https://doi.org/10.5194/bg-12-2873-2015, 2015.
Russell, A. D., Hönisch, B., Spero, H. J., and Lea, D. W.: Effects of seawater carbonate ion concentration and temperature on shell U, Mg, and Sr in cultured planktonic foraminifera, Geochim. Cosmochim. Ac. 68, 4347–4361, https://doi.org/10.1016/j.gca.2004.03.013, 2004.
Sadekov, A., Darling, K. F., Ishimura, T., Wade, C., Kimoto, K., Singh, A., Anand, P., Kroon, D., Jung, S., Ganssen, G., Ganeshram, R., Tsunogai, U., and Elderfield, H.: Geochemical imprints of genotypic variants of Globigerina bulloides in the Arabian Sea, Paleoceanography, 31, 1440–1452, https://doi.org/10.1002/2016pa002947, 2016.
Salter, S. J., Cox, M. J., Turek, E. M., Calus, S. T., Cookson, W. O., Moffatt, M. F., Turner, P., Parkhill, J., Loman, N. J., and Walker, A. W.: Reagent and laboratory contamination can critically impact sequence-based microbiome analyses, BMC Biol., 12, 87–99, https://doi.org/10.1186/S12915-014-0087-Z, 2014.
Sarmiento, J. L. and Gruber, N. (Eds): Ocean Biogeochemical Dynamics. Princeton University Press, New Jersey, 2005.
Sautter, L. R. and Thunell, R. C.: Planktonic foraminiferal response to upwelling and seasonal hydrographic conditions; sediment trap results from San Pedro Basin, Southern California Bight, J. Foramin. Res., 21, 347–363, https://doi.org/10.2113/gsjfr.21.4.347, 1991.
Scanlan, D. J., Ostrowski, M., Mazard, S., Dufresne, A., Garczarek, L., Hess, W. R., Post, A. F., Hagemann, M., Paulsen, I., and Partensky, F.: Ecological genomics of marine picocyanobacteria, Microbiol. Mol. Biol. Rev., 73, 249–299, https://doi.org/10.1128/MMBR.00035-08, 2009.
Schiebel, R.: Planktic foraminiferal sedimentation and the marine calcite budget, Global Biogeochem. Cy., 16, 1–21, https://doi.org/10.1029/2001GB001459, 2002.
Schiebel, R., Barker, S., Lendt, R., Thomas, H., and Bollmann, J.: Planktic foraminiferal dissolution in the twilight zone, Deep-Sea. Res. Pt. II, 54, 676–686, https://doi.org/10.1016/j.dsr2.2007.01.009, 2007.
Schweikert, M. and Meyer, B.: Characterization of intracellular bacteria in the freshwater dinoflagellate Peridinium cinctum, Protoplasma, 217, 177–184, https://doi.org/10.1007/BF01283398, 2001.
Seears, H., Darling, K. F., and Wade, C. M.: Ecological partitioning and diversity in tropical planktonic foraminifera, BMC Evol. Biol., 12, 54–69, https://doi.org/10.1186/1471-2148-12-54, 2012.
Six, C., Thomas, J.-C., Garczarek, L., Ostowski, M., Dufresne, A., Blot, N., Scanlan, D. J., and Partensky, F.: Diversity and evolution of phycobilisomes in marine Synechococcus spp.: a comparative genomics study, BMC Genomics, 8, R259, https://doi.org/10.1186/gb-2007-8-12-r259, 2007
Spero, H. J., Lerche, I., and Williams, D. F.: Opening the carbon isotope “vital effect” black box, 2, Quantitative model for interpreting foraminiferal carbon isotope data, Paleoceanography, 6, 639–655, https://doi.org/10.1029/91PA02022, 1991.
Spero, H. J. and Lea, D. W.: Experimental determination of stable isotope variability in Globigerina bulloides: implications for paleoceanographic reconstructions, Mar. Micropaleontol., 28, 231–246, https://doi.org/10.1016/0377-8398(96)00003-5, 1996
Spero, H. J., Bijma, J., Lea, D. W., and Bemis, B. E.: Effect of seawater carbonate concentration on foraminiferal carbon and oxygen isotopes, Nature, 390, 497–500, https://doi.org/10.1038/37333, 1997.
Stewart, D. E. and Farmer, F. H.: Extraction, identification, and quantitation of phycobiliprotein pigments from phototrophic plankton, Limnol. Oceanogr., 29, 392–397, https://doi.org/10.4319/lo.1984.29.2.0392, 1984
Suttle, C. A. and Chan, A. M.: Dynamics and distribution of cyanophages and their effect on marine Synechococcus spp., Appl. Environ. Microbiol., 60, 3167–3174, 1994.
Tai, V. and Palenik, B.: Temporal variation of Synechococcus clades at a coastal Pacific Ocean monitoring site, ISME J., 3, 903–915, https://doi.org/10.1038/ismej.2009.35, 2009.
Tai, V., Burton, R. S., and Palenik, B.: Temporal and spatial distributions of marine Synechococcus in the Southern California Bight assessed by hybridization to bead-arrays, Mar. Ecol. Prog. Ser., 426, 133–147, https://doi.org/10.3354/meps09030, 2011.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S.: MEGA6: molecular evolutionary genetics analysis version 6.0, Mol. Biol. Evol., 30, 2725–2729, https://doi.org/10.1093/molbev/mst197, 2013.
Thunell, R. and Sautter, L. R.: Planktonic foraminiferal faunal and stable isotopic indices of upwelling: a sediment trap study in the San Pedro Basin, Southern California Bight, Geol. Soc. Lond. Special Publ., 64, 77–91, https://doi.org/10.1144/GSL.SP.1992.064.01.05, 1992.
Toledo, G. and Palenik, B.: Synechococcus diversity in the California current as seen by RNA polymerase (rpoC1) gene sequences of isolated strains, Appl. Environ. Microbiol., 63, 4298–4303, 1997.
Tsuchiya, M., Toyofuku, T., Uematsu, K., Brüchert, V., Collen, J., Yamamoto, H., and Kitazato, H.: Cytologic and Genetic Characteristics of Endobiotic Bacteria and Kleptoplasts of Virgulinella fragilis (Foraminifera), J. Eukaryot. Microbiol., 62, 454–469, https://doi.org/10.1111/jeu.12200, 2015.
Uhle, M. E., Macko, S. A., Spero, H. J., Engel, M. H., and Lea, D. W.: Sources of carbon and nitrogen in modern planktonic foraminifera: the role of algal symbionts as determined by bulk and compound specific stable isotopic analyses, Org. Geochem., 27, 103–113, https://doi.org/10.1016/S0146-6380(97)00075-2, 1997.
Uhle, M. E., Macko, S. A., Spero, H. J., Lea, D. W., Ruddiman, W. F., and Engel, M. H.: The fate of nitrogen in the Orbulina universa foraminifera–symbiont system determined by nitrogen isotope analyses of shell-bound organic matter, Limnol. Oceanogr., 44, 1968–1977, https://doi.org/10.4319/lo.19126.96.36.1998, 1999.
van Hoek, A. H. A. M., van Alen, T. A., Sprakel, V. S. I., Leunissen, J. A. M., Brigge, T., Vogels, G. D., and Hackstein, J. H. P.: Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates, Mol. Biol. Evol., 17, 251–258, 2000.
Walters, W., Hyde, E. R., Berg-Lyons, D., Ackermann, G., Humphrey, G., Parada, A., Gilbert, J. A., Jansson, J. K., Caporaso, J. G., Fuhrman, J. A., Apprill, A., and Knight, R.: Improved Bacterial 16S rRNA Gene (V4 and V4-5) and Fungal Internal Transcribed Spacer Marker Gene Primers for Microbial Community Surveys, Systems, 1, e00009, https://doi.org/10.1128/mSystems.00009-15, 2015.
Waterbury, J. B., Watson, S. W., Guillard, R. R. L., and Brand, L. E.: Widespread occurrence of a unicellular, marine, planktonic, cyanobacterium, Nature, 277, 293–294, https://doi.org/10.1038/277293a0, 1979.
Wernegreen, J. J.: Genome evolution in bacterial endosymbionts of insects, Nat. Rev. Genet., 3, 850–861, https://doi.org/10.1038/nrg931, 2002.
Wolf-Gladrow, D. A., Riebesell, U., Burkhardt, S., and Bijma, J.: Direct effects of CO2 concentration on growth and isotopic composition of marine plankton, Tellus B, 51, 461–476, https://doi.org/10.1034/j.1600-0889.1999.00023.x, 1999.
Wyman, M., Gregory, R. P. F., and Carr, N. G.: Novel role for phycoerythrin in a marine cyanobacterium, Synechococcus strain DC2, Science, 230, 818–820, https://doi.org/10.1126/science.230.4727.818, 1985.
Wyman, M.: An in vivo method for the estimation of phycoerythrin concentrations in marine cyanobacteria (Synechococcus spp.), Limnol. Oceanogr., 37, 1300–1306, https://doi.org/10.4319/lo.19188.8.131.520, 1992.
Yuasa, T., Horiguchi, T., Mayama, S., Matsuoka, A., and Takahashi, O.: Ultrastructural and molecular characterization of cyanobacterial symbionts in Dictyocoryne profunda (polycystine radiolaria), Symbiosis, 57, 51–55, https://doi.org/10.1007/s13199-012-0174-2, 2012.
Accurate ecological data on planktic foraminifera (calcifying microbes that play an important role in the carbon cycle) are important for modelling their response to climate change. We studied the species G. bulloides. A lack of algal symbionts and unusual shell chemistry suggest a different life history compared to other spinose species. We demonstrate that G. bulloides hosts cyanobacterial endobionts. This has implications for modelling this species and for understanding its shell chemistry.
Accurate ecological data on planktic foraminifera (calcifying microbes that play an important...