Article

Dormancy in the foraminifera: A review

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Abstract

The Foraminifera are a diverse class of protists whose ubiquity in marine environments, small shells, and ease of collection have made them critical tools in bioindicator, bioassay, paleo-environmcntal, and paleoceanographic research. Despite the plethora of applications and accompanying literature on foraminifers, many aspects of their biology and ecology remain unexplored. One of these aspects is dormancy, a life-history strategy involving suspension of active life, arrested development, and reduced or suspended metabolic activity, mediated either by internal physiological factors (known as diapause) or exogenous factors (known as quiescence). Dormancy is a widespread adaptation, playing a role in the life cycles of a huge variety of organisms. Yet, despite anecdotal and circumstantial evidence, very little research has directly addressed this aspect of foraminiferal biology. The relatively recent discovery of cryptobiotic propagules has revealed a fundamental role for dormancy in the life cycles of foraminifers, most prominently for dispersal. Moreover, culture studies with environmental applications have shown that post-propagule quiescence (i.e., in juveniles, sub-adults and adults) may be a common response to environmental stressors, allowing rapid recovery of populations following disturbance or otherwise unfavorable conditions. A review of publications on foraminiferal biology revealed that observations indicating the potential for dormancy have been recorded for at least six decades, and that this potential is well represented throughout the class in a variety of forms, suggesting that dormancy may be a basic adaptation in the Foraminifera. If dormancy is as widespread as the literature suggests, its role in structuring foraminiferal assemblages and determining global distributions in the geological past, present, and future is fundamental. Further research into the mechanisms of dormancy will expand understanding of its role in foraminiferal life cycles, and provide new perspectives in the many fields that utilize and apply foraminiferal data.

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... While growth in athalamous species can be continuous, interrupted or slowed down by external (environmental) factors, growth in thalamous species must be stepwise, internally controlled by growth factors and externally by the environment (e.g. Bradshaw, 1957;Lee et al., 1963;Lee and Bock, 1976;Röttger, 1976;Hallock, 1981;Lombard et al., 2009;Uthike and Althenrath, 2010;Triantaphyllou et al., 2012;Langlet et al., 2013;Ross and Hallock, 2016). In monothalamous representatives with more or less spherical tests, the individuals leave the test and grow to larger size, then construct a new test (e.g. ...
... Alve and Goldstein, 2003;Goldstein and Alve, 2011). This enables survival in quiescence under unfavorable conditions for up to several years (Ross and Hallock, 2016), whereby growth starts after arrival at an appropriate habitat. ...
... They are then released to the environment after constructing several chambers and can immediately start growing, if environmental conditions remain constant. When the asexually produced gamont/ schizont propagules of smaller benthic foraminifera (inhabiting shallow water fine sediments) are transported to hostile deeper environments, they can survive several years as cryptobionts, like the sexually produced agamonts (Goldstein and Alve, 2011;Ross and Hallock, 2016). Growth starts after reposition into a favorable environment or switching to favorable conditions. ...
... Instead, the non-denitrifying species Bulimina marginata, Cassidulina laevigata, and Leptohalysis scotti dominated in this hypoxic environment. Their survival could be due to seasonal dormancy (Ross and Hallock, 2016; and their ability to release propagules which can disperse and grow when environmental conditions turn favorable again . Table S2, GF17-1A). ...
... On the other hand, the physicochemical disturbances increase the patchiness due to the variety of foraminiferal response to stress conditions . Thus, the dormant specimens and propagules wait for favorable conditions to recolonize the sediment (Alve, 1999;Alve andGoldstein, 2003, 2010;Ross and Hallock, 2016;. The challenge remains the identification of the time lag between the flood event and the response of foraminifera. ...
... Rose Bengal is the efficiency on short time scales and therefore the limitation of false positives crucial to describe population dynamics in highly transient environments Figueira et al., 2012;Pucci et al., 2009;Ross and Hallock, 2016;Melaniuk, 2021). ...
Thesis
The overall aim of this PhD thesis was to investigate sedimentary micro-environments and ecosystem functioning of two coastal areas. We combined different high spatial resolution methods and multivariate analyses at different spatio-temporal scales to reveal interactions between benthic faunal and geochemical compartments. Firstly, we investigated two stations with contrasted oxygen, nitrate and manganese conditions in the Gullmar Fjord (Sweden). We revealed the high contribution (50–100 %) of denitrifying benthic foraminifera to the nitrogen cycle in oxygenated and nitrate-rich micro–environments. Nitrogen and manganese cycles are closely related to oxygenation conditions of the ecosystem. Our results highlighted the high contribution (87 %) of macrofaunal bioirrigation to Mn release to the water column under hypoxic conditions. Secondly, we focused on a monthly monitoring of two ecological bioindicators groups; microphytobenthos (MPB) and foraminifera in the Bourgneuf Bay mudflat (France). We showed that foraminiferal reproduction events were modulated by unfavorable conditions (high hydrodynamic and winter conditions) versus favorable conditions (low hydrodynamic and summer conditions). We also demonstrated that foraminiferal species fed preferentially on diatom species based on their shape, size and life-forms. We further compared, with high spatial resolution methods, geochemical conditions at two contrasted months, which allowed to clarify the behavior of redox species and nutrients. Then, foraminiferal micro-distributions indicated the state of sediment instability versus stability. Finally, this doctoral research opens new perspectives in the use of high spatial resolution in 2D/3D to solve complex benthic ecology problems
... Bernard et al. [41] observed a decrease of the adenosine 5 0 -triphosphate (ATP) pool in foraminifera Bulimina marginata, Stainforthia fusiformis and Adercotryma glomeratum from Drammensfjord (Norway) exposed to anoxia, and suggested that this might indicate a state of dormancy. Indeed, dormancy or quiescence, defined as reduced or suspended metabolic activity in response to exogenous factors, might be a more widespread adaptation strategy of benthic foraminifera to environmental stress than previously acknowledged [42]. Even during periods with normal oxic conditions in bottom waters, foraminifera and other benthic meiofauna species can be (and frequently are) exposed to low O 2 levels simply because bioturbation mechanically moves them deeper into the sediments [43,44]. ...
... Nevertheless, anabolic processes did initially take place, conceivably driven by the 'oxic metabolic machinery' still available to the cell during the first hours after establishment of anoxic conditions. The reduced state of metabolism seems consistent with a state of dormancy or quiescence, defined as a suspension of active life, arrested development, and reduced or suspended metabolic activity [42], in our case due to the sudden onset of anoxic conditions. Consistent with a state of dormancy/ quiescence is the fact that no obvious ultrastructural damage to the cells was observed, indicating that capability to return to a state of normal vitality once oxic conditions are reestablished. ...
Article
Full-text available
High input of organic carbon and/or slowly renewing bottom waters frequently create periods with low dissolved oxygen concentrations on continental shelves and in coastal areas; such events can have strong impacts on benthic ecosystems. Among the meiofauna living in these environments, benthic foraminifera are often the most tolerant to low oxygen levels. Indeed, some species are able to survive complete anoxia for weeks to months. One known mechanism for this, observed in several species, is denitrification. For other species, a state of highly reduced metabolism, essentially a state of dormancy, has been proposed but never demonstrated. Here, we combined a 4 weeks feeding experiment, using 13 C-enriched diatom biofilm, with correlated TEM and NanoSIMS imaging, plus bulk analysis of concentration and stable carbon isotopic composition of total organic matter and individual fatty acids, to study metabolic differences in the intertidal species Ammonia tepida exposed to oxic and anoxic conditions. Strongly contrasting cellular-level dynamics of ingestion and transfer of the ingested biofilm components were observed between the two conditions. Under oxic conditions , within a few days, intact diatoms were ingested, degraded, and their components assimilated, in part for biosynthesis of different cellular components: 13 C-labeled lipid droplets formed after a few days and were subsequently lost (partially) through respiration. In contrast, in anoxia, fewer diatoms were initially ingested and these were not assimilated or metabo-lized further, but remained visible within the foraminiferal cytoplasm even after 4 weeks. Under oxic conditions, compound specific 13 C analyses showed substantial de novo synthesis by the foraminifera of specific polyunsaturated fatty acids (PUFAs), such as 20:4(n-6). Very limited PUFA synthesis was observed under anoxia. Together, our results show that anoxia induced a greatly reduced rate of heterotrophic metabolism in Ammonia tepida on a time scale of less than 24 hours, these observations are consistent with a state of dormancy.
... Thus, dispersal in form of propagules appears to be quite widespread among many species of benthic foraminifera [11,19,20]. If propagules are transported into habitats outside their normal environmental conditions, they can become dormant [21], which has also been observed in adult foraminifera [22], and can remain viable within the local propagule bank for at least two years [19]. If local environmental conditions should become suitable (e.g., due to climate change), subsequent growth of the propagules to adult populations is possible [10,19]. ...
... A temperature logger (LOG200, Dostmann electronic) was placed within one of the boxes for the monitoring of ambient temperature during the 18h transport. In May, temperatures during transport varied between [16][17][18][19][20][21][22].8˚C and in October they ranged from 17.8-22.6˚C. After arrival at the micropaleontological laboratory of the University of Bonn (Germany), the containers were opened and the suspension was left to settle for approximately 28h before being processed for the growth experiments. ...
Article
Full-text available
Foraminiferal propagule banks occur in fine sediment fractions that contain small individuals of benthic foraminifera. These sediments include locally sourced juveniles and propagules, as well as allochthonous propagules that have dispersed from surrounding areas. Such propagules can remain viable even under unfavorable local conditions. When exposed to more favorable conditions, they may grow to adult stages. Accordingly, during environmental changes, propagule banks have the potential to function as species pools and allow quick assemblage reactions. The propagule method was designed to study responses of foraminiferal assemblages by exposing propagule banks to controlled conditions in the laboratory, an approach that is applicable to a variety of ecological questions. Therefore it is important to understand the nature and dynamics of propagule banks, including local and seasonal influences. To obtain insights into the composition of local propagule banks, we studied experimentally grown assemblages from two shallow-water lagoons on Corfu Island in western Greece, and compared the results with in situ assemblages. We sampled in spring and autumn of 2017 and experimental treatments included the use of different substrates in our experiments to account for potential effects on assemblage compositions. Results revealed that sediments from each lagoon contained a distinct propagule bank. We found abundant allochthonous taxa among specimens grown in all experimental treatments, indicating dispersal of propagules, and possibly also juveniles, from adjacent regions into both lagoons. The time of sampling had a significant effect on experimental assemblages, indicating that the composition of propagule banks can vary throughout the year. However, no significant differences were found in assemblages grown in different substrata, suggesting a stronger influence of water variables (e.g., temperature or salinity) on assemblage compositions. Moreover, the experimental set-ups favored small, fast-growing, sediment-dwelling species tolerant of relatively high organic content. Our findings highlight the potential of propagule banks as species pools and will help to refine and improve future applications of the method.
... Lunar periodicity in standing stocks, size, and shell flux has been observed in numerous species of planktic foraminifera (37,38), attributed to the need for synchrony in gametogenesis to allow gametes to meet and fuse. Therefore, low and varying degrees of lunar periodicity between populations and species, size classes within species, and through time (39) are difficult to explain with obligatory sexual reproduction but are readily explained by the occurrence of facultative sexual and asexual reproduction as shown here. ...
... We propose that some species have a slow-growing, sexually produced generation that disperses much farther than their faster-growing asexually reproduced counterparts. This dynamic may be partially analogous to the propagule hypothesis for benthic foraminifera, where juveniles that are more frequently the product of sexual reproduction can maintain dormancy until conditions become suitable for growth (39,40). ...
Article
Full-text available
Marine protists are integral to the structure and function of pelagic ecosystems and marine carbon cycling, with rhizarian biomass alone accounting for more than half of all mesozooplankton in the oligotrophic oceans. Yet, understanding how their environment shapes diversity within species and across taxa is limited by a paucity of observations of heritability and life history. Here, we present observations of asexual reproduction, morphologic plasticity, and ontogeny in the planktic foraminifer Neogloboquadrina pachyderma in laboratory culture. Our results demonstrate that planktic foraminifera reproduce both sexually and asexually and demonstrate extensive phenotypic plasticity in response to nonheritable factors. These two processes fundamentally explain the rapid spatial and temporal response of even imperceptibly low populations of planktic foraminifera to optimal conditions and the diversity and ubiquity of these species across the range of environmental conditions that occur in the ocean.
... denitrification; Risgaard-Petersen et al., 2006;Piña-Ochoa et al., 2010a), to sequester chloroplast (i.e. kleptoplastidy; Jauffrais et al., 2018), to associate with bacterial symbionts (Bernhard et al., 2010) or to enter into a state of dormancy (Ross and Hallock, 2016;LeKieffre et al., 2017). ...
... The bottom panel shows the total living foraminiferal abundances for both replicates (grey bars), mean abundances (diamonds) and standard deviations (black error bars) calculated for the two replicates, for all investigated months (in bold) in 2011 and 2012. mancy (Ross and Hallock, 2016;LeKieffre et al., 2017) to deal with low-oxygen conditions. Concerning the species found in this study, although the presence of intracellular nitrate was shown for Ammonia, denitrification tests yielded negative results (Piña-Ochoa et al., 2010a;Nomaki et al., 2014). ...
Article
Full-text available
Over the last decades, hypoxia in marine coastal environments has become more and more widespread, prolonged and intense. Hypoxic events have large consequences for the functioning of benthic ecosystems. In severe cases, they may lead to complete anoxia and the presence of toxic sulfides in the sediment and bottom-water, thereby strongly affecting biological compartments of benthic marine ecosystems. Within these ecosystems, benthic foraminifera show a high diversity of ecological responses, with a wide range of adaptive life strategies. Some species are particularly resistant to hypoxia–anoxia, and consequently it is interesting to study the whole foraminiferal community as well as species-specific responses to such events. Here we investigated the temporal dynamics of living benthic foraminiferal communities (recognised by CellTracker™ Green) at two sites in the saltwater Lake Grevelingen in the Netherlands. These sites are subject to seasonal anoxia with different durations and are characterised by the presence of free sulfide (H2S) in the uppermost part of the sediment. Our results indicate that foraminiferal communities are impacted by the presence of H2S in their habitat, with a stronger response in the case of longer exposure times. At the deepest site (34 m), in summer 2012, 1 to 2 months of anoxia and free H2S in the surface sediment resulted in an almost complete disappearance of the foraminiferal community. Conversely, at the shallower site (23 m), where the duration of anoxia and free H2S was shorter (1 month or less), a dense foraminiferal community was found throughout the year except for a short period after the stressful event. Interestingly, at both sites, the foraminiferal community showed a delayed response to the onset of anoxia and free H2S, suggesting that the combination of anoxia and free H2S does not lead to increased mortality, but rather to strongly decreased reproduction rates. At the deepest site, where highly stressful conditions prevailed for 1 to 2 months, the recovery time of the community takes about half a year. In Lake Grevelingen, Elphidium selseyense and Elphidium magellanicum are much less affected by anoxia and free H2S than Ammonia sp. T6. We hypothesise that this is not due to a higher tolerance for H2S, but rather related to the seasonal availability of food sources, which could have been less suitable for Ammonia sp. T6 than for the elphidiids.
... Moreover, it was shown that this foraminifer was becoming active in the presence of food. Thus, it could be hypothesized that the large size of some G. biora and T. earlandi specimens could predispose them for surviving long periods of food deficiency, perhaps in dormancy, see Ross & Hallock (2016) for an overview of this special behavior in foraminifera. ...
... Development of dense, long spines observed in some T. earlandi specimens (e.g., Fig. 5a) was definitely genetically controlled. In the view of possible dormancy, in this foraminifer (Ross & Hallock, 2016) long spines might be defensive. They could also resemble spines in planktonic foraminifera, which help to increase buoyancy and support pseudopods to expose symbionts to daylight and free gas exchange with oceanic water (Hemleben et al., 1989). ...
Article
Habitats proximal to grounded ice and below ice shelves are rarely studied for microfossils. A recently described, well-resolved deglaciation record from the Whales Deep Basin of the eastern Ross Sea provided an opportunity to study sub-fossil foraminifera in such settings. Among other foraminiferal taxa, two forms with pustulose/spinose ornamentation were especially important as they were restricted to habitats associated with proximity to the calving front or presence of an ice-shelf. Based on gradation from strongly pustulose/spinose to typical morphologies and existing molecular data, these rarely reported forms are considered to be morphotypes of Globocassidulina biora (Crespin, 1960) and Trifarina earlandi (Parr, 1950). They seemed to flourish in polynya areas near grounding-line and in sub-ice-shelf environments with bottom currents. Their unusual morphologies may be a response to limited food resources. These foraminifera deserve special attention because they appear to be restricted to extreme Antarctic environments and hence are potentially very important for paleoenvironmental reconstructions.
... Ross & Hallock (2014) explored the use of an LBF, Amphistegina gibbosa d'Orbigny, as a bioassay organism in toxicological studies relevant to coral reefs. During the development of protocols to determine the 48-hr 50% lethal concentration (LC50) of propylene glycol and 2-butoxyethanol (components of dispersants used in the Deepwater Horizon oil spill), we observed that A. gibbosa specimens were capable of surviving some level of toxic exposure by entering a dormant state, in which live individuals were visually indistinguishable from dead individuals, showing no signs of activity, which includes extension of the granuloreticulopodia, attachment to substrate, or production of visible waste (see Ross & Hallock, 2016, for further discussion and definition of dormancy in the Foraminifera). The identification of truly dead specimens required the use of a 72-hr recovery period to determine visually which individuals showed no evidence of activity. ...
... However, the uncertainty in the resulting LC50 estimates indicated the need for other readily applicable methods for determining mortality. Though seldom considered by researchers, dormancy is widespread among the Foraminifera (see Ross & Hallock, 2016, and references therein). Previous observations of dormancy in A. gibbosa under aphotic conditions (Smith & Hallock, 1992) reinforced the need to distinguish dormant from dead individuals and to better understand physiological facets of dormancy. ...
Article
Full-text available
The uses of fluorescent microscopy and fluorescent probes, such as the metabolically activated probe CellTracker™ Green CMFDA (CTG), have become common in studies of living Foraminifera. This metabolic requirement, as well as the relatively quick production of the fluorescent reaction products, makes CTG a prime candidate for determining mortality in bioassay and other laboratory experiments. Previous work with the foraminifer Amphistegina gibbosa , which hosts diatom endosymbionts, has shown that the species is capable of surviving both acute chemical exposure and extended periods of total darkness by entering a low-activity dormant state. This paper explores the use of CTG and fluorescent microscopy to determine mortality in such experiments, as well as to explore the physiology of dormant foraminifers. The application of CTG was found to be complicated by the autofluorescence of the diatom symbionts, which masks the signal of the CTG, as well as by interactions between CTG and propylene glycol, a chemical of interest known to cause dormancy. These complications necessitated adapting methods from earlier studies using CTG. Here we present observations on CTG fluorescence and autofluorescence in A. gibbosa following both chemical exposure and periods of total darkness. While CTG can indicate vital activity in dormant foraminifers, complications include underestimates of total survival and recovery, and falsely indicating dead individuals as live due to rapid microbial colonization. Nonetheless, the brightness of the CTG signal in dormant individuals exposed to propylene glycol supports previously published results of survival patterns in A. gibbosa . Observations of CTG fluorescence in individuals kept for extended periods in aphotic conditions indicate uptake of CTG may begin within 30 min of exposure to light, suggesting darkness-induced dormancy and subsequent recovery can occur on short time scales. These results suggest that CTG accurately reflects changes associated with dormancy, and can be useful in laboratory experiments utilizing symbiont-bearing foraminifers.
... Lunar periodicity in standing stocks, size, and shell flux has been observed in numerous species of planktic foraminifera (37,38), attributed to the need for synchrony in gametogenesis to allow gametes to meet and fuse. Therefore, low and varying degrees of lunar periodicity between populations and species, size classes within species, and through time (39) are difficult to explain with obligatory sexual reproduction but are readily explained by the occurrence of facultative sexual and asexual reproduction as shown here. ...
... We propose that some species have a slow-growing, sexually produced generation that disperses much farther than their faster-growing asexually reproduced counterparts. This dynamic may be partially analogous to the propagule hypothesis for benthic foraminifera, where juveniles that are more frequently the product of sexual reproduction can maintain dormancy until conditions become suitable for growth (39,40). ...
... Dormancy commonly involves the suspension of active life, arrested development, reduced or suspended metabolic activity, and the ability to recover from these conditions (i.e., Cáceres, 1997;Guidetti et al., 2011;Lennon and Jones, 2011). Some manifestation of dormancy is found across a wide variety of taxa, including plants, mammals, fish, and reptiles (see Ross and Hallock, 2016, and references therein) and especially among protistan groups, including marine protists such as dinoflagellates (e.g., Binder and Anderson, 1990;Figueroa et al., 2007;Smayda and Trainer, 2010;Lundholm et al., 2011;Bravo and Figueroa, 2014) and diatoms (e.g., Smetacek, 1985;McQuoid and Hobson, 1996;Lewis et al., 1999;von Dassow and Montresor, 2010). O'Farrell (2011) considers cellular quiescence to be a fundamental, primitive adaptation to survive resource limitations inherent to rapid generation times; its presence in "primitive" single-celled organisms is nearly ubiquitous. ...
... Until recently, few studies have directly addressed dormancy in the Foraminifera. Nevertheless, a review of foraminiferal research concluded that dormancy appears to be a common adaptation across this phylum as well (Ross and Hallock, 2016). Dormancy has been suggested as a survival response to a number of environmental triggers in the Foraminifera, including temperature (Bradshaw, 1957), anoxia (Bernhard, 1993;Bernhard and Alve, 1996;Moodley et al., 1997;Nomaki et al., 2016;LeKieffre et al., 2017;Koho et al., 2018), anoxia with accompanying reducing conditions (Bernhard, 1993;Langlet et al., 2013Langlet et al., , 2014, and toxic chemical exposure (McCloskey, 2009;Hallock, 2014, 2018) photosymbiotic species, such as Amphistegina spp. ...
Article
Dormancy in the Foraminifera has been observed widely across the phylum in reaction to a variety of triggers including, in the diatom symbiont-bearing foraminifer Amphistegina gibbosa, extended periods of darkness. Resumption of activity in the host-symbiont holobiont was noted, but not fully documented, in specimens reintroduced to light following up to 12 months in darkness. Here, criteria for documenting recovery included resumption of reticulopodial activity in the host and return of pre-treatment golden-brown color characteristic of an active symbiotic diatom population. Reticulopodial activity resumed in nearly all treatment specimens (>95%) following 12 months in darkness, and in >70% of the specimens when reintroduced to light following 20 months in darkness. Image analysis using the percent of the foraminiferal surface area showing golden-brown color as a proxy for recovery of the endosymbionts showed return of such color within days for shorter treatments (7 and 12 months in darkness), but slower and less complete return in longer treatments (15 and 20 months), indicating increased susceptibility to photic damage of symbionts as the length of dormancy increased.
... Later, Kitazato & Matsushita (1996) demonstrated the same biphasic life cycle for T. hadai in laboratory cultures. Dormancy also occurs in some foraminifera (Alve & Goldstein, 2002Goldstein & Alve, 2011; see review in Ross & Hallock, 2016), particularly in response to stressed environmental conditions due to low temperature (10-15°C) or high salinity (ࣙ50 psu) (i.e., Ammonia tepida in Bradshaw, 1957Bradshaw, , 1961; anoxia (Bernhard, 1993;Bernhard & Alve, 1996;Moodley et al., 1997); chemical exposure (McCloskey, 2009;Ross & Hallock, 2014); or extended darkness (Smith & Hallock, 1992). Although a resting stage has not been proven for T. hadai specifically, the species' ability to seasonally colonize severely stressed environments (e.g., Matsushita & Kitazato, 1990;Choi & An, 2012) suggests it is capable of this survival strategy as well. ...
Article
We investigated the potential role of ballast sediment from coastal and transoceanic oil tankers arriving and de-ballasting in Port Valdez as a vector for the introduction of invasive benthic foraminifera in Prince William Sound, Alaska. Forty-one ballast sediment samples were obtained during 1998–1999 from 11 oil tankers that routinely discharged their ballast in Prince William Sound after sailing from other West Coast (Los Angeles/Long Beach Harbor, San Francisco Bay, and Puget Sound) or foreign ports (Japan, Korea, and China) where they originally ballasted. Forty of these samples contained benthic foraminifera, including 27 (66%) with the introduced species Trochammina hadai Uchio from nine (81%) of the ships. In all, 59 species were recovered and foraminiferal abundance peaked at 27,000 specimens per gram dry sediment. Of the 41 samples, three were stained and living benthic foraminifera were recovered in all three of them. The entrained foraminifera reflected the number of times ballasting occurred (single or multiple sources), the location of ballasting (estuarine or offshore), and post-acquisition alteration of the sediment (i.e., growth of gypsum crystals at the possible expense of calcareous tests). In temperate regions, sediment samples resulting from single-source ballasting in estuaries (SSBE), multiple-source ballasting in estuaries (MSBE), single-source ballasting offshore (SSBO), and a combination of SSBO and SSBE or MSBE, typically contained increasingly higher species richness, respectively. The potential for foreign species invasion is dependent on the presence of viable candidates and their survivability, their abundance in the ballasting location, and the number of times ballasting occurs, most of which are evident from the ship's ballasting history. We estimate that 442.1 billion to 8.84 trillion living foraminifera were introduced into Port Valdez in a single year, suggesting it is quite likely that an invasive species could be successfully established there. Trochammina hadai is a good example of a successful invasive in Prince William Sound for the following reasons: 1) the species is abundant enough in U.S. West Coast and foreign ports where ballasting occurs that sufficient individuals needed for reproduction may be transported to the receiving waters; 2) Port Valdez, in particular, receives repeated and frequent inoculations from the same source ports where T. hadai is present; 3) large quantities of sediment are taken up by commercial vessels during ballasting and benthic foraminifera occur in abundance in ballast sediment; 4) ballast sediment provides a suitable environment in which benthic foraminifera can survive for extended periods of time during transport; 5) T. hadai flourishes in a wide range of temperatures and environmental conditions that characterize both the ports where ballasting takes place as well as in Port Valdez where de-ballasting occurs; and 6) the species is capable of asexual reproduction and possibly the ability to form a dormant resting stage, both of which have the potential to lower the threshold for colonization. Clearly, ballast sediment is a viable vector for the introduction of T. hadai and other invasives into Alaskan ports and elsewhere worldwide.
... In benthic foraminifera, resettlement by propagules that can rest for months or years under unfavorable conditions in fine-grained sediments, starting growth when conditions become favorable, is important in shallow marine environments (Alve andGoldstein 2002, 2003). Beside these propagules, other types of dormancy during life-time allows survival under unfavorable conditions (Ross and Hallock 2016). ...
Article
Full-text available
Living (LAs) and death assemblages (DAs) from the same samples (sites) can be compared based on total densities, species densities, species richness and heterogeneity (evenness). Preferably densities (standing crop), obtained by normalization of absolute frequencies to unit sample size, should be used to compare samples, especially for LAs. Combinations of the above four characteristics enable a better insight into the relations between LAs and DAs. The 'Incorporation Value'weighs the proportions of living individuals on total individual numbers with similarities in species composition between both assemblages, yielding the instantaneous integration grade of living individuals into the death assemblage. Diversity diagrams based on species richness (abscissa) and heterogeneities (ordinate), standardized over all investigated samples, simultaneously characterize differences in diversities. The standardized vector between LA and DA in the above-mentioned coordinate system characterizes differences in species richness and heterogeneity in a combined manner, where all coefficients of species richness and heterogeneities can be used.
... In order to cope with low oxygen concentrations, benthic foraminifera have developed a range of mechanisms such as nitrate respiration 8,26,27 , sequestration of chloroplasts 28,29 , bacterial symbionts 21 , ultrastructural adaptations 20,21 or dormancy 30,31 . However, Ammonia was shown unable to sequester chloroplasts 29 and seems strictly aerobic 31 . ...
Article
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Due to climate warming and increased anthropogenic impact, a decrease of ocean water oxygenation is expected in the near future, with major consequences for marine life. In this context, it is essential to develop reliable tools to assess past oxygen concentrations in the ocean, to better forecast these future changes. Recently, foraminiferal pore patterns have been proposed as a bottom water oxygenation proxy, but the parameters controlling foraminiferal pore patterns are still largely unknown. Here we use scaling laws to describe how both gas exchanges (metabolic needs) and mechanical constraints (shell robustness) control foraminiferal pore patterns. The derived mathematical model shows that only specific combinations of pore density and size are physically feasible. Maximum porosity, of about 30%, can only be obtained by simultaneously increasing pore size and decreasing pore density. A large empirical data set of pore data obtained for three pseudocryptic phylotypes of Ammonia, a common intertidal genus from the eastern Atlantic, strongly supports this conclusion. These new findings provide basic mechanistic understanding of the complex controls of foraminiferal pore patterns and give a solid starting point for the development of proxies of past oxygen concentrations based on these morphological features. Pore size and pore density are largely interdependent, and both have to be considered when describing pore patterns.
... Benthic foraminiferal propagules can be widely distributed by waves and currents (Alve andGoldstein 2003, 2010). Particularly, Ross and Hallock (2016) proposed that cosmopolitan species produce propagules with great potential for dispersal, while endemic taxa may have lost this basic characteristic. Current patterns in the adjacent Skagerrak area are dominated by the northward Baltic Current, which flows from the Kattegat -along the Swedish west coast (where Gullmar and Sannäs fjords are located) towards the entrance of the outer Oslofjord. ...
Article
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Specimens resembling the benthic foraminifera Nonionella stella (Cushman and Moyer, 1930), a morphospecies originally described from the San Pedro Basin, California, USA, were observed for the first time in the Oslofjord (Norway) in 2012. This study investigates the Oslofjord Nonionella population in order to confirm its non-indigenous species (NIS) status and assess its introduction time. Morphological characterisation based on SEM imaging complemented by molecular identification using small subunit (SSU) rDNA sequencing and assessment of the recent past record (sediment core), were performed on material collected in the Oslofjord in 2016. Examination of the dead fauna showed that specimens resembling N. stella only appeared recently in the Oslofjord, confirming the NIS status of this population. Moreover, DNA results indicate that the Oslofjord specimens differ genetically from N. stella sampled in the Santa Barbara Basin (California USA). Hence, we propose to use the name Nonionella sp. T1 for the specimens sampled in the Oslofjord for the time being. In the southern part of the Skagerrak, specimens morphologically similar to Nonionella sp. T1 were reported as NIS in the Gullmar fjord (Sweden) in 2011 and in the Skagerrak in 2015. Molecular data indicate that the two populations from Gullmar-and Oslofjords are identical, based on their SSU rDNA sequences. In addition, analyses of foraminiferal dead assemblages suggest that the population from the Gullmar fjord settled prior to the Oslofjord population, i.e. ~ 1985 and about 2010, respectively. This implies that Nonionella sp. T1 may have been transported from Sweden to Norway by northward coastal currents.
... Some specimens can be colorful and even appear to be alive when the cells are dead and the DNA is already partly degraded. On the other hand, some cells appear to be dead when in fact they are dormant (Ross & Hallock, 2016). Some DNA extracts contain products that can inhibit PCR amplification. ...
Article
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We carried out a series of experiments to evaluate the efficiency of preserving DNA from porcelaneous foraminifera (Quinqueloculina spp.) and a second set to assess the effect of Rose Bengal staining on molecular processing. The first experimental setup assessed three methods of DNA preservation (air-drying, freezing with or without seawater, and Guani-dine lysis buffer treatment with or without EDTA (Ethylene-diaminetetraacetic acid)). Our study produced the following results: 1) there were no significant differences in DNA preservation when samples were air dried across a range of temperatures (20-120°C); samples frozen at -20°C appeared better preserved than at those frozen at -80°C, and freezing without seawater appeared to produce better preservation than with seawater, though differences in freezing treatments were not significant (p > 0.05); samples in Guanidine lysis buffer with EDTA and stored at -20°C were well preserved (p < 0.05); 2) sometimes, DNA was successfully extracted from samples stained with Rose Bengal. We recommend Guanidine lysis buffer with EDTA, stored at -20°C for up to six weeks, as the best protocol for preservation of DNA from porcelaneous foraminifera.
... While the temperature was only 28 • C when samples were collected, the potential range of temperatures at this very shallow (<2 m) location can vary seasonally from lows of ∼17 • C in winter to as high as 40 • C in summer (Joydas et al., 2015). Thus, any organisms that live at this site either must be able to a) tolerate such extremes, b) recruit from propagules produced during times of milder conditions or carried into the bay by currents or migrating birds (e.g., Weinmann & Goldstein, 2016), or c) utilize post-propagule dormancy (Ross & Hallock, 2016) to survive seasonal extremes. ...
Article
The Arabian Gulf is considered a naturally stressed environment due to extremes of salinity and summer temperatures, and the Salwa Bay area is commonly considered to be the most hypersaline extension of this gulf. This study documents foraminiferal diversity, abundance and incidences of test deformities in Salwa Bay, near the Saudi Arabia−Qatar Border. The total time-averaged (live + dead) benthic foraminiferal assemblage was dominated by porcelaneous taxa (85%). The three most abundant specieswerePeneroplis pertusus (24%), P. planatus (15%), and Coscinospira hemprichii (9%), accounting for nearly half of the total assemblage. Other common taxa included Elphidium spp. (14%), Ammonia spp. (10%), and Quinqueloculina sp. (4%). About a quarter of the specimens picked were living (rose Bengal stained) at the time of collection, and 43% of the tests of the most common taxa were mildly to severely deformed. Types of deformities included fusion of two adults or double tests, protuberances on the spiral side, abnormal chamber arrangement, abnormal shape of the proloculus, dents, re-positioning of the aperture, and modification of the coiling plane. Two genera accounted for three quarters of the observed test deformities: Peneroplis (58%) and Coscinospira (17%). The combination of elevated temperatures, high salinities, and the ecology of the taxa encountered is likely responsible for the abundance, relatively low diversity, and high incidence of deformities in foraminiferal tests from Salwa Bay.We conclude that the percentage of test abnormalities is not a useful environmental proxy for pollution in such naturally stressed environments where high incidences of test deformities commonly occur.
... In addition, dispersal by tidal currents (e.g., Arslan et al., 2016b) into the highly corrosive conditions in deeper zones of TL are likely to dissolve the foraminiferal tests, which would contribute to low FD values, and to changes in distribution and dominance. Dormancy is another factor to consider since reports have shown that propagules remain in stasis until environmental conditions are more favorable (Alve and Goldstein, 2003;Ross and Hallock, 2016) which could also be the case in the deeper portions of TL. ...
Article
Torrecillas Lagoon, on the north coast of Puerto Rico, has experienced extensive anthropogenic influence over the past 200 years. Elevated concentrations of Potentially Toxic Elements (PTEs) in bulk sediment (Cu, Zn, Pb, Ni, Cr, Li, V, Fe, As, Se, and Mn) have been reported in surficial sediments and have relatively uniform spatial distributions. Areas with higher concentrations are associated with a higher percentage of total organic carbon (TOC) and percent mud (mud), as well as anoxic conditions. Ammonia beccarii, Quinqueloculina rhodiensis, and Triloculina oblonga are the dominant foraminifers in the lagoon and are characteristic of stressed coastal environments. Bulk concentrations of Cu-Zn-Fe are negatively correlated with numerous foraminiferal taxa, absolute abundances, and diversity indices, though very few correlations with the bioavailable counterparts (F2 Tess-bioavailable) are observed. Similarly, relative abundances of Quinqueloculina and Triloculina positively correlate with bulk Cu-Zn-Fe but not with F2 Tess-bioavailable. The waters in Torrecillas lagoon show strong stratification, with hypoxic/anoxic (dissolved oxygen <3 mg/L) and corrosive (pH < 7.4) conditions below 4 m depth. The presence of such strong gradients in very shallow water represents a dynamic chemical environment, with changes occurring on day-night cycles, tidal cycles, and especially with storm activity that induces mixing of otherwise highly stratified, very localized waters. Recognizing the potential for sequestered PTEs to be re-mobilized is an essential insight for coastal management agencies that must assess the risks of existing PTEs during coastal engineering activities (e.g., dredge and fill activities) and major storm events. Exchangeable and oxidizable fractions are likely more bioavailable than acid-soluble fractions in influencing the ecology of for-aminifers under most circumstances.
... (phylotype T6, = Ammonia tepida of LeKieffre et al., 2017) decreases its metabolism and enters dormancy under anoxia. Dormancy or reduced metabolism could be a widespread response in benthic foraminifera to survive unfavorable conditions (e.g., anoxia) (Ross and Hallock, 2016). This coping mechanism could be especially common for shallow-water foraminifera living in dynamic environments, like subtidal and intertidal settings, which experience frequent changes in pore water chemistry associated with tidal action (e.g., Taillefert et al., 2007). ...
Article
The ultrastructure of the living foraminiferan, Ammonia sp. (phylotype unknown), collected from surficial and deeper, subsurface (anoxic) sediments from the Dutch Wadden Sea, was examined to provide information on the physiology of the foraminiferal cell and its adaptive strategies to low oxygen conditions. The observed changes in cell ultrastructure under anoxia were further compared with the cell ultrastructure of Ammonia sp. (phylotype T6), from oxic and anoxic incubation experiments. The ultrastructural evidence indicates that under low oxygen conditions Ammonia spp. may accumulate lipid droplets. In addition, the size of the lipid droplets may increase with the duration of anoxic conditions, becoming over 5. μm in size, while the remaining cytosol of the foraminiferan become less electron dense. In some specimens, lipid droplets were also found in the space between the plasma membrane and the organic lining. We expect that the apparent increase in the number and size of the lipid droplets is indicative of a stress response of the foraminifera to the adverse anoxic conditions. Other ultrastructural changes in response to anoxia include the presence of intact bacteria and electron dense opaque bodies within the foraminiferal cytosol, and a possible thickening of the organic lining. The role of the bacteria remains enigmatic but they may be linked to foraminiferal dormancy in anoxia.
... Instead, the non-denitrifying species Bulimina marginata, Cassidulina laevigata, and Leptohalysis scotti dominated in this hypoxic environment. Their survival could be due to seasonal dormancy (Ross and Hallock, 2016;LeKieffre et al., 2017). The suspected deep nitrification zone (blue square profile, Fig. 6 h) could explain the presence of nitrate micro-niches deeper in the sediment and might explain the patchy distribution of 360 ...
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Oxygen availability impacts the marine nitrogen cycle at a range of spatial and temporal scales. Invasive organisms have shown to sustainably affect sediment geochemistry and benthic ecology. Nonionella sp. T1 was recently described as an invasive benthic foraminifer in the North Sea region. Here, we demonstrate the impact of this denitrifying species on the foraminifera fauna and the nitrogen cycle of the Gullmar Fjord (Sweden). The foraminifera contribution to benthic denitrification was estimated by coupling living foraminifera micro-distribution, denitrification rate measurement and sedimentary nitrate 2D distribution. Nonionella sp. T1 dominated the foraminifera fauna and could denitrify up to 50–100 % of nitrate porewater in oxygenated bottom waters of the fjord. Contrastingly, at the deepest hypoxic low-nitrate station, denitrifying foraminifera species were scarce and did not contribute to nitrogen removal (~ 5 %). Our study showed that benthic foraminifera can be a major contributor of nitrogen mitigation in oxic coastal ecosystems and should be included in ecological and diagenetic models aiming at understanding biogeochemical cycles coupled to nitrogen.
... The diatom endosymbionts of A. gibbosa, shown in transmission electron micrographs by Talge and Hallock (2003), are~3 μm in diameter, Contributions of Trimorphic Life Cycles to Dispersal and Evolutionary Trends in Large Benthic Foraminifers comparable in size to a foraminiferal zygote. Dormant stages occur in chlorophyte, dinoflagellate and diatom lineages (e. g., Ross and Hallock, 2016;Fryxell, 1983; and references in both), so cryptobiotic propagules could include algal cells. In Peneroplis spp., the rhodophyte cells are functionally organelles rather than endosymbionts, and are also in the 3-4 μm diameter range (e. g., Lee, 1990). ...
Article
The basic life cycle of Foraminifera has long been recognized as alternation between sexual and asexual generations; a common modification is several successive asexual generations. Production and release of flagellated gametes also has been documented as the basic sexual-reproductive mode in extant lineages. Research on population dynamics, local spatial distributions, and biogeography of Amphistegina spp. and Heterostegina depressa have been augmented by culture studies over the past 50 years, providing insights that have been widely used in paleoecological and paleoenvironmental interpretations. Hypotheses are proposed suggesting how stages in the life cycle might contribute to understanding biogeographic and evolutionary trends commonly observed in large benthic foraminifers. Recruitment of sexually-produced cryptobiotic propagules, followed by successive asexual generations (schizogeny), can potentially establish viable, locally-adapted populations within literally years, consistent with the concepts of both allopatric speciation and reticulate evolution associated with isolation and reconnection of local basins. The review concludes with the recommendation that future studies utilizing genomics, proteonomics, geochemistries, scanning technologies, and other approaches can promote greater understanding of both modern and fossil larger benthic foraminiferal lineages.
... In addition, foraminifera display a large spectrum of size in natural environment (Murray & Alve 2000, Alve & Murray 2001, Murray 2006, Geslin et al. 2011, Cesbron et al. 2016. For instance, individuals can range from micrometres to millimetres in size length within a species (Murray 1983, Caralp 1989, Alve & Goldstein 2003, Ross & Hallock 2016. In chapter I (Deldicq et al. revised; see Chapter I, Part 2 for further details), it is shown that the contribution of five intertidal foraminiferal species to surface sediment reworking is more controlled by species-specific motion traits rather than by size. ...
Thesis
The aim of this PhD is to describe the role of benthic foraminifera in bioturbation processes focusing on particulate fluxes at the sediment-water interface. Specifically, the objectives are fourfold: (i) characterising the motion behaviour of key benthic foraminiferal species inhabiting intertidal mudflats from the Eastern English Channel at the sediment water interface to further classify them into functional groups of bioturbation, (ii) quantifying surface sediment reworking rates of the above-mentioned species, (iii) understanding how biotic and abiotic parameters may drive the mode and the intensity of surface sediment reworking of the dominant species Haynesina germanica, and (iv) further describing the vertical burrowing dynamics and the biogenic structures built by Haynesina germanica to quantify its bioturbation rates. To do so, the following parameters are described: the travelled distance, the velocity, the vertical position, the activity level and the tortuosity of the path. The motion-behaviour is described for the following species: Haynesina germanica, Cribroelphidium williamsoni, Quinqueloculina seminulum, Ammonia tepida and Miliammina fusca. Although they are all classified in the functional group of biodiffusors, these species differ in their preferential vertical position within the sediment. Specifically, C. williamsoni is an epifaunal-biodiffusor, Q. seminulum, M. fusca and H. germanica are gallery-biodiffusors while A. tepida is a surficial biodiffusor. This therefore means that the mode of sediment reworking is species-specific in benthic foraminifera. Its intensity is mediated by specific traits as well as biotic and abiotic factors. Indeed, travelled distance, velocity, activity level and tortuosity of the path would vary between and within species. As a consequence, the rate and the mode of sediment reworking are species-, individual- and functional group-dependant. Specifically, the surface area of the test, the species density, the temperature and the organic matter concentration are key parameters that control the bioturbation activity of H. germanica. The present work highlights the role of benthic foraminifera in sediment reworking processes taking place at the sediment-water interface and in the sediment column. It opens new perspectives on the understanding of the ecology of foraminifera and their putative non-negligible role in bioturbation processes in intertidal ecosystems.
... In fact, a fundamental point in these kinds of studies is to distinguish dead foraminifera versus survivors. Previous work (Ross and Hallock, 2016;Ross, 2012) reported that foraminifera can survive a stressful condition by entering a low activity dormant state, looking to be dead. This life-strategy could affect the experiment results causing underestimated survivors, therefore the CTG was used to overcome this problem. ...
Article
Cigarette butts are the most common form of litter in the world and their environmental impact is related to both persistence and potential toxic effects for chemical composition. The objective of this study was to assess the acute toxicity (LC50-48 h) of human-smoked cigarette butts leachate on 3 cultured genera of benthic foraminifera: the calcareous perforate Rosalina globularis, the calcareous imperforate Quinqueloculina spp., and the agglutinated Textularia agglutinans. The specimens were exposed to 16, 8, 4, 2, and 1 cigarette butts/L concentrations that prove to be acutely toxic to all taxa. Starting from 4 cigarette butts/L, both calcareous genera showed shell decalcification, and death of almost all the individuals, except for the more resistant agglutinated species. These results suggest the potential harmfulness of cigarette butts leachate related to pH reduction and release of toxic substances, in particular nicotine, which leads to physiology alteration and in many cases cellular death.
... Among marine protists, benthic foraminifera are nearly ubiquitous in aquatic environments where they represent up to 47% of the eukaryotic benthic biomass and, therefore, represent a major component of the meiofauna in marine sediments (e.g., Gooday et al., 2000;Moodley et al., 2000;Pascal et al., 2009). These organisms exhibit diverse life strategies, including heterotrophy, bacterial and/or algal symbioses, kleptoplasty (sequestered chloroplasts), anaerobic (nitrate) respiration, and dormancy (e.g., Goldstein, 1999;Nomaki et al., 2006;Jauffrais et al., 2016;Bernhard et al., 2018;Piña-Ochoa et al., 2010a;Ross and Hallock, 2016). This diversity of life strategies enables them to colonize a wide variety of benthic environments, where they are often considered substantial contributors to nitrogen biogeochemical cycling (Høgslund et al., 2008;Piña-Ochoa et al., 2010a;Glock et al., 2013;Choquel et al., 2021). ...
Article
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Nitrogen and sulfur are key elements in the biogeochemical cycles of marine ecosystems to which benthic foraminifera contribute significantly. Yet, cell-specific assimilation of ammonium, nitrate and sulfate by these protists is poorly characterized and understood across their wide range of species-specific trophic strategies. For example, detailed knowledge about ammonium and sulfate assimilation pathways is lacking and although some benthic foraminifera are known to maintain intracellular pools of nitrate and/or to denitrify, the potential use of nitrate-derived nitrogen for anabolic processes has not been systematically studied. In the present study, NanoSIMS isotopic imaging correlated with transmission electron microscopy was used to trace the incorporation of isotopically labeled inorganic nitrogen (ammonium or nitrate) and sulfate into the biomass of twelve benthic foraminiferal species from different marine environments. On timescales of twenty hours, no detectable ¹⁵ N-enrichments from nitrate assimilation were observed in species known to perform denitrification, indicating that, while denitrifying foraminifera store intra-cellular nitrate, they do not use nitrate-derived nitrogen to build their biomass. Assimilation of both ammonium and sulfate, with corresponding ¹⁵ N and ³⁴ S-enrichments, were observed in all species investigated (with some individual exceptions for sulfate). Assimilation of ammonium and sulfate thus can be considered widespread among benthic foraminifera. These metabolic capacities may help to underpin the ability of benthic foraminifera to colonize highly diverse marine habitats.
... Benthic foraminifera have a ubiquitous and cosmopolitan distribution in marine sediments and include representatives that display a variety of ecological adaptations (e.g., facultative anaerobes, dormancy, symbiosis) (e.g., Ross and Hallock, 2016) that may make them sensitive or more resilient to natural or anthropogenic environmental stressors. Numerous studies have reported the ecological responses of benthic foraminifera in recent sediments to both inorganic contaminants like potentially toxic elements (PTEs) and persistent organic pollutants (POPs, e.g., pesticides) (Martínez-Colón et al., 2009;Suokhrie et al., 2017), lending support for their applicability as proxies to assess the negative effects of environmental stressors. ...
Article
This work documents the presence of potentially toxic elements (PTEs) in the sediment and in tests of Ammonia tepida, one of the most common benthic foraminifera species in coastal environments worldwide. It aims to analyze if the presence of PTEs in the carbonate test of this species is related to metals concentration in the sediment aiming its application in paleoenvironmental studies. Three chambers of fifty A. tepida specimens from contaminated and uncontaminated sediments from the Sepetiba Bay, one of the most polluted coastal systems from the SE Brazil, were analyzed using an Environmental Scanning Electron Microscope coupled with an X-ray Dispersive Energy Spectrometer. The results reveal the presence of lithogenic elements and PTEs in the tests of A. tepida. Relatively high values of Pb, Hg and Sn were found in specimens recovered from both polluted and unpolluted sediment layers. The bioaccumulation index revealed higher enrichment of Cd and Cr in tests from sediments moderately to heavily polluted by Cd and to a lesser extent by Cr. The results suggest that the incorporation of metals might be controlled and affected by several factors, such as the water residence time, availability of the metals, and biogeochemical processes. As a result, applications of this method utilizing A. tepida for paleoenvironmental studies do not appear to be feasible without further research.
... P rotists are single-celled eukaryotes of astounding morphological and functional diversity inhabiting virtually every life-harboring niche on this planet. These microorganisms have complex life cycles comprising stages of distinct phenotypic traits (e.g., morphology, cell size, cystic/vegetative status, and growth rate), which undergo changes in response to fluctuating environmental variables (1)(2)(3)(4)(5)(6). Recently, the advent of sequencing technologies has greatly facilitated the study of ribotypic traits, i.e., the qualitative and quantitative attributes of rRNA genes (ribosomal DNA [rDNA]) and/or rRNA transcripts, which are used to assess protistan diversity and community composition in natural ecosystems (7). ...
Article
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Relationships between ribotypic and phenotypic traits of protists across life-cycle stages remain largely unknown. Herein, we used single cells of two soil and two marine ciliate species to examine phenotypic and ribotypic traits and their relationships across lag, log, plateau, cystic stages and temperatures. We found that Colpoda inflata and C. steinii demonstrated allometric relationships between 18S rDNA copy number per cell (CNPC), cell volume (CV), and macronuclear volume across all life-cycle stages. Integrating previously reported data of Euplotes vannus and Strombidium sulcatum indicated taxon-dependent rDNA CNPC–CV functions. Ciliate and prokaryote data analysis revealed that the rRNA CNPC followed a unified power-law function, only if the rRNA-deficient resting cysts were not considered. Hence, a theoretical framework was proposed to estimate the relative quantity of resting cysts in the protistan populations with total cellular rDNA and rRNA copy numbers. Using rDNA CNPC was a better predictor of growth rate at a given temperature than rRNA CNPC and CV, suggesting replication of redundant rDNA operons as a key factor that slows cell division. Single-cell high throughput sequencing and analysis after correcting sequencing errors revealed multiple rDNA and rRNA variants per cell. Both encystment and temperature affected the number of rDNA and rRNA variants in several cases. The divergence of rDNA and rRNA sequence in a single cell ranged from 1% to 10%, depending on species. These findings have important implications for inferring cell-based biological traits (e.g., species richness, abundance and biomass, activity, and community structure) of protists using molecular approaches. Importance: Based on phenotypic traits, traditional surveys usually characterize organismal richness, abundance, biomass, and growth potential to describe diversity, organization and function of protistan populations and communities. The ribosomal RNA gene (rDNA) and its transcripts have been widely used as molecular markers in ecological studies of protists. Nevertheless, the manner in which these molecules relate to cellular (organismal) and physiological traits remains poorly understood, which could lead to misinterpretations of protistan diversity and ecology. The current research highlights the dynamic nature of cellular rDNA and rRNA contents, which tightly couple with multiple phenotypic traits in ciliated protists. We demonstrate that quantity of resting cysts and maximum growth rate of a population can be theoretically estimated using ribotypic trait-based models. The intra-individual sequence polymorphisms of rDNA and rRNA can be influenced by encystment and temperature, which should be considered when interpreting species-level diversity and community structure of microbial eukaryotes.
... The observation of survival without growth is consistent with the concept of 'dormancy', observed among different species of foraminifera under various stress conditions (Ross & Hallock, 2016). In our case, the 'dormancy' is only manifested by lack of growth, while metabolic activity is maintained. ...
Article
Global warming permits range expansions of tropical marine species into mid‐latitude habitats, where they are, however, faced with cold winter temperatures. Therefore, tolerance to cold temperatures may be the key adaptation controlling zonal range expansion in tropical marine species. Here we investigated the molecular and physiological response to cold and heat stress in a tropical symbiont‐bearing foraminifera that has successfully invaded the Eastern Mediterranean. Our physiological measurements indicate thermal tolerance of the diatom symbionts but a decrease of growth for the foraminifera host under both cold and warm stress. The combined (“holobiont”) transcriptome revealed an asymmetric response in short‐term gene expression under cold versus warm stress. Cold stress induced major reorganization of metabolic processes, including regulation of genes involved in photosynthesis. Analyses limited to genes that are inferred to belong to the symbionts confirm that the observed pattern is due to changes in the regulation of photosynthesis‐related genes and not due to changes in abundance of the symbionts. In contrast to cold stress, far fewer genes change expression under heat stress and those that do are primarily related to movement and cytoskeleton. This implies that under cold stress, cellular resources are allocated to the maintenance of photosynthesis, and the key to zonal range shifts of tropical species could be the cold tolerance of the symbiosis.
... The endospore may exist for centuries, during which time they "exhibit complete metabolic dormancy and extreme resistance to multiple environmental insults" (Mury and Popham, 2014). A similar resistant state, known as a cyst, resting egg, or resting stage, is also common in a variety of protists (Corliss, 2001;Ross and Hallock, 2016), and phyto- (Ribeiro et al., 2011;Ellegaard and Ribeiro, 2018) and zooplankton (Gilbert, 1974;Ricci, 2001). ...
Article
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Dormancy is an inactive period of an organism's life cycle that permits it to survive through phases of unfavorable conditions in highly variable environments. Dormancy is not binary. There is a continuum of dormancy phenotypes that represent some degree of reduced metabolic activity (hypometabolism), reduced feeding, and reduced reproduction or proliferation. Similarly, normal cells and cancer cells exhibit a range of states from quiescence to long-term dormancy that permit survival in adverse environmental conditions. In contrast to organismal dormancy, which entails a reduction in metabolism, dormancy in cells (both normal and cancer) is primarily characterized by lack of cell division. "Cancer dormancy" also describes a state characterized by growth stagnation, which could arise from cells that are not necessarily hypometabolic or non-proliferative. This inconsistent terminology leads to confusion and imprecision that impedes progress in interdisciplinary research between ecologists and cancer biologists. In this paper, we draw parallels and contrasts between dormancy in cancer and other ecosystems in nature, and discuss the potential for studies in cancer to provide novel insights into the evolutionary ecology of dormancy.
... incertum: [51]), as well as dormancy inside of a protective cyst (or not) during unfavorable conditions such as anoxia (E. incertum: [51,69]), reduced temperature (Ammonia tepida: [68]), temperature and chemical exposure (Amphistegina gibbosa: [70,71]), or extended darkness [72]. ...
Article
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Transitional waters straddle the interface between marine and terrestrial biomes and, among others, include fjords, bays, lagoons, and estuaries. These coastal systems are essential for transport and manufacturing industries and suffer extensive anthropogenic exploitation of their ecosystem services for aquaculture and recreational activities. These activities can have negative effects on the local biota, necessitating investigation and regulation. As a result of this, EcoQS (ecological quality status) assessment has garnered great attention as an essential aspect of govern- mental bodies’ legislative decision-making process. Assessing EcoQS in transitional water ecosystems is problematic because these systems experience high natural variability and organic enrichment and often lack information about their pre-human impact, baseline, or “pristine” reference conditions, knowledge of which is essential to many commonly used assessment methods. Here, foraminifera can be used as environmental sentinels, providing ecological data such as diversity and sensitivity, which can be used as the basis for EcoQS assessment indices. Fossil shells of foraminifera can also provide a temporal aspect to ecosystem assessment, making it possible to obtain reference conditions from the study site itself. These foraminifera-based indices have been shown to correlate not only with various environmental stressors but also with the most common macrofaunal-based indices currently employed by bodies such as the Water Framework Directive (WFD). In this review, we firstly discuss the development of various foraminifera-based indices and address the challenge of how best to implement these synergistically to understand and regulate human environmental impact, particularly in transitional waters, which have historically suffered disproportionate levels of human impact or are difficult to assess with standard EcoQS methods. Further, we present some case studies to exemplify key issues and discuss potential solutions for those. Such key issues include, for example, the disparate performance of multiple indices applied to the same site and a proper assignment of EcoQS class boundaries (threshold values) for each index. Disparate aptitudes of indices to specific geomorphologic and hydrological regimes can be leveraged via the development of a site characteristics catalogue, which would enable the identification of the most appropriate index to apply, and the integration of multiple indices resulting in more representative EcoQS assessment in heterogenous transitional environments. In addition, the difficulty in assigning threshold values to systems without analogous unimpacted reference sites (a common issue among many transitional waters) can be overcome by recording EcoQS as an ecological quality ratio (EQR). Lastly, we evaluate the current status and future potential of an emerging field, genetic biomonitoring, focusing on how these new techniques can be used to increase the accuracy of EcoQS assessment in transitional systems by supplementing more established morphology-based methods.
... and the first occurrence (Campanian) of V. munieri may somewhat suggest homeomorphism rather than a phyletic relation. However, in our opinion it is reasonable assuming that through such a transitional time some "ghost" Vandenbroeckia (ghost ranges; Wills, 2007) were present in shallow seas, possibly thriving in dormancy (Ross and Hallock, 2016). This assumption is in accordance with the supposed r-strategy of Vandenbroeckia causae sp. ...
Article
The Cenomanian-Turonian boundary represents a time of biotic changes affecting the diversity of larger foraminifera in shallow-water carbonate platform facies. Apart of the several taxa that suffered extinction, there is an additional cluster showing some stratigraphic occurrences before and after the CTB. Here we report a further example from the Cenomanian of the Mount Pastrik (Albanian-Kosovan boundary) that is represented by a new species within the Peneroplidae, Vandenbroeckia causae sp. nov. So far, representatives of this genus were only reported from the Campanian and Maastrichtian. The retrieval of Vandenbroeckia before CTB suggests that the genus escaped the extinction, re-appearing in the uppermost Cretaceous under a renewed specific status.
... The length of time foraminiferal propagules remain viable in sediments is unknown, but one study showed that propagules grew after 2 years in adverse conditions (Alve and Goldstein, 2010). Additionally, dormancy, which has been documented in foraminifera (reviewed in Ross and Hallock, 2016), can bolster their persistence as a group. ...
Article
Ocean chemistry is changing as a result of human activities. Atmospheric carbon dioxide (CO2) concentrations are increasing, causing an increase in oceanic pCO2 that drives a decrease in oceanic pH, a process called ocean acidification (OA). Higher CO2 concentrations are also linked to rising global temperatures that can result in more stratified surface waters, reducing the exchange between surface and deep waters; this stronger stratification, along with nutrient pollution, contributes to an expansion of oxygen-depleted zones (so called hypoxia or deoxygenation). Determining the response of marine organisms to environmental changes is important for assessments of future ecosystem functioning. While many studies have assessed the impact of individual or paired stressors, fewer studies have assessed the combined impact of pCO2, O2, and temperature. A long-term experiment (∼10 months) with different treatments of these three stressors was conducted to determine their sole or combined impact on the abundance and survival of a benthic foraminiferal community collected from a continental-shelf site. Foraminifera are well suited to such study because of their small size, relatively rapid growth, varied mineralogies and physiologies. Inoculation materials were collected from a ∼77-m deep site south of Woods Hole, MA. Very fine sediments (<53 μm) were used as inoculum, to allow the entire community to respond. Thirty-eight morphologically identified taxa grew during the experiment. Multivariate statistical analysis indicates that hypoxia was the major driving factor distinguishing the yields, while warming was secondary. Species responses were not consistent, with different species being most abundant in different treatments. Some taxa grew in all of the triple-stressor samples. Results from the experiment suggest that foraminiferal species’ responses will vary considerably, with some being negatively impacted by predicted environmental changes, while other taxa will tolerate, and perhaps even benefit, from deoxygenation, warming and OA.
... Based on this observation, foraminifera might feel uncomfortable at low salinities and react to this with M. Lintner et al.: The effect of the salinity, light regime and food source on C and N uptake a reduced metabolism. There are a few studies which discuss the reduction of metabolism due to stressful conditions (Bernhard and Alve, 1996;Ross and Hallock, 2016;LeKieffre et al., 2017). This may lead to a generally lower activity of foraminifera, which reduces their cell respiration and results in a lower C output. ...
Article
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Foraminifera are unicellular organisms that play an important role in marine organic matter cycles. Some species are able to isolate chloroplasts from their algal food source and incorporate them as kleptoplasts into their own metabolic pathways, a phenomenon known as kleptoplastidy. One species showing this ability is Elphidium excavatum, a common foraminifer in the Kiel Fjord, Germany. The Kiel Fjord is fed by several rivers and thus forms a habitat with strongly fluctuating salinity. Here, we tested the effects of the food source, salinity and light regime on the food uptake (via 15N and 13C algal uptake) in this kleptoplast-bearing foraminifer. In our study E. excavatum was cultured in the lab at three salinity levels (15, 20 and 25) and uptake of C and N from the food source Dunaliella tertiolecta (Chlorophyceae) and Leyanella arenaria (Bacillariophyceae) were measured over time (after 3, 5 and 7 d). The species was very well adapted to the current salinity of the sampling region, as both algal N and C uptake was highest at a salinity of 20. It seems that E. excavatum coped better with lower than with higher salinities. The amount of absorbed C from the green algae D. tertiolecta showed a tendency effect of salinity, peaking at a salinity of 20. Nitrogen uptake was also highest at a salinity of 20 and steadily increased with time. In contrast, C uptake from the diatom L. arenaria was highest at a salinity of 15 and decreased at higher salinities. We found no overall significant differences in C and N uptake from green algae vs. diatoms. Furthermore, the food uptake at a light–dark rhythm of 16:8 h was compared to continuous darkness. Darkness had a negative influence on algal C and N uptake, and this effect increased with incubation time. Starving experiments showed a stimulation of food uptake after 7 d. In summary, it can be concluded that E. excavatum copes well with changes of salinity to a lower level. For changes in light regime, we showed that light reduction caused a decrease of C and N uptake by E. excavatum.
... However, benthic foraminifera are widely understood to be among the ex-tremophiles that thrive in the OMZ through special adaptations (Levin, 2003;Bernhard and Bowser, 2008;Glock et al., 2012Glock et al., , 2018Glock et al., , 2019LeKieffre et al., 2017;Gooday et al., 2020). Benthic foraminiferal adaptations include nitrate respiration (Risgaard-Petersen et al., 2006;Hogsland et al., 2008;Pina-Ochoa et al., 2010;Bernhard et al., 2011Bernhard et al., , 2012aWoehle et al., 2018;Orsi et al., 2020), dormancy (Bernhard and Alve, 1996;Ross and Hallock, 2016;LeKieffre et al., 2017), and morphologies consistent with facilitating increased gas exchange (Bernhard, 1986;Perez-Cruz and Machain-Castillo, 1990;Glock et al., 2011Glock et al., , 2012Kuhnt et al., 2013Kuhnt et al., , 2014Rathburn et al., 2018). There they are important contributors to benthic food webs (e.g., Nomaki et al., 2008;Enge et al., 2014) and are used as indicators of low-oxygen environments (e.g., Kaiho, 1994;Bernhard et al., 1997;Cannariato et al., 1999;Jorissen et al., 2007;Ohkushi et al., 2013). ...
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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 depth-stratified plankton tows to demonstrate that some species of planktic foraminifera are adapted to life in the heart of the pelagic oxygen minimum zone (OMZ). In particular, we identify two species, Globorotaloides hexagonus and Hastigerina parapelagica, living within the eastern tropical North Pacific OMZ. The tests of the former are preserved in marine sediments and could be used to trace the extent and intensity of low-oxygen pelagic habitats in the fossil record. Additional morphometric analyses of G. hexagonus show that tests found in the lowest oxygen environments are larger, more porous, less dense, and have more chambers in the final whorl. The association of this species with the OMZ and the apparent plasticity of its test in response to ambient oxygenation invites the use of G. hexagonus tests in sediment cores as potential proxies for both the presence and intensity of overlying OMZs.
... Since the propagules can be transported well outside their natural distribution ranges, ''exotic'' species regularly appear within these experiments Goldstein 2003, 2010;Goldstein and Alve 2011;Goldstein 2016, 2017;Weinmann et al. 2019). Propagules outside of their natural environment can become dormant Goldstein 2002, 2010;Ross and Hallock 2016) but can be ready to grow and become a part of local assemblages as soon as the conditions change in their favor, as has been suggested from field observations (Schönfeld 2018;Hart et al. 2020). As such, propagule banks provide useful tools to study the effect of different parameters on the composition and structure of foraminiferal assemblages. ...
... Since the propagules can be transported well outside their natural distribution ranges, ''exotic'' species regularly appear within these experiments Goldstein 2003, 2010;Goldstein and Alve 2011;Goldstein 2016, 2017;Weinmann et al. 2019). Propagules outside of their natural environment can become dormant Goldstein 2002, 2010;Ross and Hallock 2016) but can be ready to grow and become a part of local assemblages as soon as the conditions change in their favor, as has been suggested from field observations (Schönfeld 2018;Hart et al. 2020). As such, propagule banks provide useful tools to study the effect of different parameters on the composition and structure of foraminiferal assemblages. ...
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Calcifying organisms such as benthic foraminifera are susceptible to changes in ocean pH and alkalinity. Responses to these changes include variations in mortality, calcification rates or assemblage composition, which have been observed in field and experimental studies. Here we applied a growth experiment with benthic foraminiferal propagules under different pH conditions to gather insights into the effect of pH on the composition of grown assemblages. A homogeneous propagule assemblage from a local mudflat in Corfu Island (Greece) was exposed to a range of pH conditions (6.5, 7.2, 7.8 and 8.5) for 5 weeks. In a second experiment, the assemblages were first exposed to low and subsequently to high conditions for a total of 8 weeks. After termination of the experiments, we recorded high survivability and growth throughout the treatments. Analysis of the assemblage composition of the first experiments revealed a shift from porcelaneous dominated taxa in the higher pH treatments to an assemblage with higher numbers of agglutinated taxa in the lower pH treatments. Soft-shelled monothalamous species were common throughout. The second experiment revealed assemblages that were significantly dominated by porcelaneous taxa with monothalamous taxa being almost absent. The results of this study are congruent with other observations on changing assemblage compositions with changing pH from both laboratory and field studies. The fast response of the assemblages through activation of potentially dormant propagules adds insights into the mechanisms behind seasonal composition changes in naturally variable environments such as river estuaries. They also shed new light on possible effects of continuous decreases in ocean pH on shallow-water foraminiferal assemblages in future.
... O'Farrell, 2011). Moreover, quiescence is not limited to foraminiferal propagules (Ross & Hallock, 2016, and references therein). For example, Bernhard (1993Bernhard ( , 1996 documented anoxia-induced quiescence in a variety of foraminiferal taxa. ...
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... Instead, the non-denitrifying species Bulimina marginata, Cassidulina laevigata, and Leptohalysis scotti dominated in this hypoxic environment. Their survival could be due to seasonal dormancy (Ross and Hallock, 2016;LeKieffre et al., 2017) and their ability to release propagules, which can disperse and grow when environmental conditions turn favorable again (Alve and Goldstein, 2003). The suspected deep nitrification zone (blue square profile, Fig. 5h) could indicate the presence of nitrate micro-niches deeper in the sediment and might explain the patchy distribution of Nonionella sp. ...
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Oxygen and nitrate availabilities impact the marine nitrogen cycle at a range of spatial and temporal scales. Here, we demonstrate the impact of denitrifying foraminifera on the nitrogen cycle at two oxygen and nitrate contrasting stations in a fjord environment (Gullmar Fjord, Sweden). Denitrification by benthic foraminifera was determined through the combination of specific density counting per microhabitat and specific nitrate respiration rates obtained through incubation experiments using N2O microsensors. Benthic nitrate removal was calculated from submillimeter chemical gradients extracted from 2D porewater images of the porewater nitrate concentration. These were acquired by combining the DET technique (diffusive equilibrium in thin film) with chemical colorimetry and hyperspectral imagery. Sediments with high nitrate concentrations in the porewater and oxygenated overlying water were dominated by the non-indigenous species (NIS) Nonionella sp. T1. Denitrification by this species could account for 50 %–100 % of the nitrate loss estimated from the nitrate gradients. In contrast sediments below hypoxic bottom waters had low inventories of porewater nitrate, and denitrifying foraminifera were rare. Their contribution to benthic nitrate removal was negligible (< 5 %). Our study showed that benthic foraminifera can be a major contributor to nitrogen mitigation in oxic coastal ecosystems and should be included in ecological and diagenetic models aiming to understand biogeochemical cycles coupled to nitrogen.
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Over the last decades, hypoxia in marine coastal environments have become more and more widespread, prolonged and intense. These hypoxic events have large consequences for the functioning of benthic ecosystems. They profoundly modify early diagenetic processes involved in organic matter recycling, and in severe cases, they may lead to complete anoxia and presence of toxic sulphides in the sediment and bottom water, thereby severely affecting biological compartments of benthic marine ecosystems. Within these ecosystems, benthic foraminifera show a high diversity of ecological responses, with a wide range of adaptive life strategies. Some species are particularly resistant to hypoxia/anoxia and consequently, it is interesting to study the whole foraminiferal community as well as species specific responses to such events. Here we investigated the temporal dynamics of living benthic foraminiferal communities (recognised by CellTracker™ Green) at two sites in the saltwater Lake Grevelingen in the Netherlands. These sites are subject to seasonal anoxia with different durations and are characterised by the presence of free sulphide (H2S) in the uppermost part of the sediment. Our results indicate that foraminiferal communities are impacted by the presence of H2S in their habitat, with a stronger response in case of longer exposure times. At the deepest site (34 m), one to two months of anoxia and free H2S in the surface sediment resulted in an almost complete disappearance of the foraminiferal community. Conversely, at the shallower site (23 m), where the duration of anoxia and free H2S was shorter (one month or less), a dense foraminiferal community was found throughout the year. Interestingly, at both sites, the foraminiferal community showed a delayed response to the onset of anoxia and free H2S, suggesting that the combination of anoxia and free H2S does not lead to increased mortality, but rather to strongly decreased reproduction rates. At the deepest site, where highly stressful conditions prevailed for one to two months, the recovery time of the community takes about half a year. In Lake Grevelingen, Elphidium selseyense and Elphidium magellanicum are much less affected by anoxia and free H2S than Ammonia sp. T6. We hypothesise that this is not due to a higher tolerance of H2S, but rather related to the seasonal availability of food sources, which could have been less suitable for Ammonia sp. T6 than for the elphidiids.
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The 4GFOR model presented in this paper combines the OMEXDIA model of Soetaert et al. (1996) with four theoretical species of benthic foraminifera. The geochemical part of the model simulates the succession of early diagenetic redox reactions in the superficial sediment layers. The four theoretical foraminiferal species, which each represent a group of biological species with comparable microhabitats, differ by their limitations with respect to oxygen and nitrate concentration and their ability to feed on different organic matter types. The foraminiferal model is a transformation model in which different proportions of four types of organic matter with different reactivity are attributed to each of the theoretical species. The model has been manually tuned and tested on a large data set from two stations, at 1000 and 550 m depth, in the Bay of Biscay. The model adequately simulates the vertical distribution of shallow, intermediate and deep infaunal species. The 4GFOR model can be used to test several hypotheses concerning foraminiferal ecology. The model has already allowed us to conclude that it is high unlikely that shallow infaunal taxa feed exclusively on the most labile part of the organic matter flux, since it was unable to reproduce the field observations while using this hypothesis. Another important conclusion based on our preliminary model results is that the absence of deep infaunal taxa close to the sediment surface may be explained by their decreasing competitiveness in well oxygenated environments. In the future, the inversion of the 4GFOR model may yield a powerful paleoceanographic tool, enabling us to reconstruct major limiting environmental factors (oxygen and nitrate concentrations; quantity and quality of the organic flux to the ocean floor) from benthic foraminiferal assemblage data.
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Heavy metal exposure from anthropogenic pollutants negatively affects many marine organisms, including foraminiferan protists. As such, foraminifera are often used as bioindicators of stressed environmental conditions. Primary research has commonly focused on how heavy metals affect foraminiferal assemblages, ultrastructure, and shell morphology; however, little if any data have been reported on how heavy metals affect their physiological functions. Here we measure respiration rates of individual foraminifera after acute exposure to three concentrations of toxic but sub-lethal levels of lead (Pb) and cadmium (Cd). These experiments relied on the large cell size of an agglutinated Antarctic foraminifer, Astrammina rara. Cells were isolated from sediment collected by scuba divers in Explorers Cove, Antarctica. In the laboratory, individual, live cells were removed from their shells and placed in sealed respirometry chambers with either normal or Pb- or Cd-spiked artificial seawater. Cells in the process of shell formation were used to ensure that all individuals were aerobically active and in similar metabolic states. Noninvasive oxygen-sensing optode technology was used to measure oxygen consumption during the first 24–36 h of shell formation. The average respiration rate was 1.07 nmol O2 h⁻¹ (range 0.78–1.84 nmol O2 h⁻¹) for normal cells. We compared the results from each exposure group to this baseline rate and found that both Pb and Cd significantly suppressed the respiration rate of A. rara in all but the highest level of Pb exposure. This study provides a novel, powerful, and short-term way to measure foraminiferal physiological responses to heavy metal toxicants.
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This study presents the first direct evidence, based on biochemical analysis of fresh material, that certain benthic foraminifera feed selectively on specific components of seasonally deposited phytodetritus in their natural environment. Three abundant species of benthic foraminifera, the calcareous species Globocassidulina subglobosa and Quinqueloculina seminula and the agglutinated species Thurammina albicans, collected after the deposition of phytoplankton bloom material at a shelf site (560 m water depth) west of the Antarctic Peninsula in March 2001, showed significant differences in their fatty acid profiles compared to the surrounding phytodetritus. Furthermore, the 2 calcareous species contained significantly higher amounts of polyunsaturated fatty acids (PUFAs) than were found in their presumptive phytodetrital food source, indicating that the foraminifera discriminate between, and selectively feed on, the different components of the deposited material. Possible implications for the benthic food web are discussed.
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Foraminifera are commonly defined as marine testate protists, and their diversity is mainly assessed on the basis of the morphology of their agglutinated or mineralized tests. Diversity surveys based on environmental DNA (eDNA) have dramatically changed this view by revealing an unexpected diversity of naked and organic-walled lineages as well as detecting foraminiferal lineages in soil and freshwater environments. Moreover, single-cell analyses have allowed discrimination among genetically distinctive types within almost every described morphospecies. In view of these studies, the foraminiferal diversity appeared to be largely underestimated, but its accurate estimation was impeded by the low speed and coverage of a cloning-based eDNA approach. With the advent of high-throughput sequencing (HTS) technologies, these limitations disappeared in favor of exhaustive descriptions of foraminiferal diversity in numerous samples. Yet, the biases and errors identified in early HTS studies raised some questions about the accuracy of HTS data and their biological interpretation. Among the most controversial issues affecting the reliability of HTS diversity estimates are (1) the impact of technical and biological biases, (2) the sensitivity and specificity of taxonomic sequence assignment, (3) the ability to distinguish rare species, and (4) the quantitative interpretation of HTS data. Here, we document the lessons learned from previous HTS surveys and present the current advances and applications focusing on foraminiferal eDNA. We discuss the problems associated with HTS approaches and predict the future trends and avenues that hold promises for surveying foraminiferal diversity accurately and efficiently. © 2014 Marine Biological Laboratory.
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A propagule experiment was designed to investigate the effects of different food types and varying sediment depths on the survival and growth of upper-bathyal benthic foraminifera, collected from surface-sediment cores in Oslofjord, Norway. Sediment that passed through a 53-μm sieve was used in the experiment. Any foraminifera >63 μm at the end of the experiment had therefore grown, indicating at least tolerable living conditions. The experiment was arranged into four sub-experiments to test foraminiferal responses to a lack of food input, algal medium, sediment depth (1- vs. 2-cm depth), and different food types. Potential food sources included monospecific algal cultures (the green alga Dunaliella tertiolecta, the haptophyte Emiliania huxleyi, and the diatoms Chaetoceros sp. and cf. Navicula), as well as phytoplankton and zooplankton from net hauls collected at the same sampling site. After six weeks all foraminiferal assemblages showed an increase in abundance, even those which were not fed. This suggests that most species (e.g., Textularia earlandi, Bathysiphon flexilis) were feeding on microbes or detritus already in the sediment. However, the addition of certain phytodetritus increased the abundance, suggesting that some species (e.g., Epistominella vitrea) are dependent on the input of this particular fresh phytodetritus. Conversely, certain types of detritus (E. huxleyi and zooplankton) appear detrimental to most species, except Elphidium excavatum which appeared resistant to the treatments inimicable to other species. Leptohalysis catella was the only species observed to respond positively to net hauls dominated by dinoflagellates. For some species (e.g., Stainforthia fusiformis, Nonionella iridea) the availability of a greater sediment depth stimulates growth more than the input of organic matter.
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Most of the photosynthetically produced organic material reaching the ocean-floor is transported as settling particles, among which larger particles such as faecal pellets and macroaggregates (marine snow) are particularly important. Recent studies in the northeastern Atlantic have demonstrated that macroaggregates originating from the euphotic zone settle at a rate of approximately 100-150 m d-1 to form a deposit (phytodetritus) on the sediment surface. Bacteria and protozoa (flagellates and foraminifers) rapidly colonize and multiply on phytodetritus, while large deposit feeding animals ingest it. Other inputs, for example Sargassum, wood and vertebrate carcasses, also evoke a rapid response by benthic organisms. However, the taxa that respond depend on the form of the organic material. The intermittent or seasonally pulsed nature of phytodetritus and many other inputs regulate the population dynamics and reproductive cycles of some responding species. These are often opportunists that are able to utilize ephemeral food resources and, therefore, undergo rapid fluctuations in population density. In addition, the patchy distribution of much of the organic material deposited on the ocean-floor probably plays a major role in structuring deep-sea benthic ecosystems.
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The life cycle of many dinoflagellates includes at least one nonflagellated benthic stage (cyst). In the literature, the different types of dinoflagellate cysts are mainly defined based on morphological (number and type of layers in the cell wall) and functional (long-or short-term endurance) differences. These characteristics were initially thought to clearly distinguish pellicle (thin-walled) cysts from resting (double-walled) dinoflagellate cysts. The former were considered short-term (temporal) and the latter long-term (resting) cysts. However, during the last two decades further knowledge has highlighted the great intricacy of dinoflagellate life histories, the ecological significance of cyst stages, and the need to clarify the functional and morphological complexities of the different cyst types. Here we review and, when necessary, redefine the concepts of resting and pellicle cysts, examining both their structural and their functional characteristics in the context of the life cycle strategies of several dinoflagellate species.
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Anoxia was successfully induced in four benthic chambers installed at 24m depth on the northern Adriatic seafloor from 9 days to 10 months. To accurately determine whether benthic foraminifera can survive experimentally induced prolonged anoxia, the CellTracker™ Green method was applied and calcareous and agglutinated foraminifera were analyzed. Numerous individuals were found living at all sampling times and at all sampling depths (to 5 cm), supported by a ribosomal RNA analysis that revealed that certain benthic foraminifera were active after 10 months of anoxia. The results show that benthic foraminifera can survive up to 10 months of anoxia with co-occurring hydrogen sulfides. However, foraminiferal standing stocks decrease with sampling time in an irregular manner. A large difference in standing stock between two cores sampled under initial conditions indicates the presence of a large spatial heterogeneity of the foraminiferal faunas. An unexpected increase in standing stocks after one month is tentatively interpreted as a reaction to increased food availability due to the massive mortality of infaunal macrofaunal organisms. After this, standing stocks decrease again in cores sampled after 2 months of anoxia to then attain a minimum in the cores sampled after 10 months. We speculate that the trend of overall decrease of standing stocks is not due to the adverse effects of anoxia and hydrogen sulfides but rather due to a continuous diminution of labile organic matter.
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Marsh foraminiferal faunas from nine cores in two transects in and around Nanaimo inlet were examined to assess the implications of infaunal habitat and taphonomic processes for biofacies formation. High marsh faunas live slightly deeper infaunally compared to those in the low marsh, reflecting harsher conditions in the high marsh. Most living Jadammina macrescens occur from 0-20 cm in the high marsh and from 0-11 cm in the low marsh; the main depth preference is from 2-8 cm. Most living Trochammina inflata occur between 0-25 cm in the high marsh and from 0-20 cm in the low marsh. Haplophragmoides wilberti is most abundant overall between 3-7 cm, being almost absent at the surface in all cores. H. wilberti is found primarily between 0-15 cm in the high marsh, and from 0-12 cm in the low marsh. Most living Miliammina fusca occur from 0-10 cm, with maximum abundance in the top 3 cm. Five cluster analyses of the foraminiferal data using a sample base of 0-1, 0-3, 0-5, 0-7 and 0-10 cm, respectively, discriminated five biofacies in each case, which were then used to determine which near-surface aliquot is most analogous to deeper subsurface biofacies. Results show near-surface sediment sampling should be done through the 0-10 cm interval. This aliquot allows the main infaunal species characteristics to be observed, yet is thin enough that epifaunal species are also accurately represented. These results indicate that at least in coastal British Columbia traditional sampling strategies that assess modern marsh foraminiferal occurrence based only on examination of the uppermost 0-1 cm will not give an accurate representation of actual marsh species distribution. Modern marsh foraminiferal distribution assessment based on the thicker surface interval that we propose will permit researchers to delineate both subtle and dramatic sea level changes more precisely. This precision is critical not only in studies designed to differentiate the magnitude of seismic events but also to recognize subtle relative sea level change events as well.
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It is generally assumed that the first fossil appearance of a group of organisms corresponds to its evolutionary origin. But we have molecular evidence that extant members of the most abundant microfossil-forming group, the Foraminifera, include `naked' amoeboid species, indicating that ancestral foraminiferans could be unfossilized. This means that the origin of the group might be much earlier than has been deduced from the fossil record. This might help to explain the conflicting molecular and fossil data on the origin of the Foraminifera.
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Sediment samples from Scottish coastal sites, taken over the last 9 years, were stored in closed containers at 5°C. Slurry cultures were used to determine the survival of phytoplankton in these sediments. A range of diatom and dinoflagellate species survived for at least 27 months in these stored samples. A number of species grew for which no resting stage has yet been described: Thalas- siosira angulata, T.pacifica, T.punctigera, T.eccentrica, T.minima and T.anguste-lineata. Notable results were survival times of 73 months for Skeletonema costatum, 96 months for Chaetoceros socialis, C.didymus and C.diadema, 109 months for Scrippsiella sp. and 112 months for Lingulo- dinium polyedrum. A single sample was stored and repeatedly cultured for diatoms over a period of 16 months. The number of species cultured from the sediment declined over this time. Lingulo- dinium polyedrum cysts isolated from sediments collected at least 18 months previously gave a hatching success of 97% and cysts isolated from a 9-year-old sample gave a hatching success of 3%. The study indicates the potential importance of coastal sediments as a source of phytoplankton to their overlying waters. The validity of using marine planktonic diatoms and dinoflagellates for modelling geological events is discussed.
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Sediments collected from the northwestern Adriatic Sea (Mediterranean) were exposed to anoxic bottom-water conditions for more than 2 mo in order to examine the resistance of dominant meiobenthic taxa to prolonged anoxia. Copepods appeared to be most sensitive to anoxia, with densities being reduced to zero within 11 d. Compared to oxic conditions, densities of both nematodes and soft-shelled foraminifera were significantly lower under prolonged anoxia. In contrast, total hard-shelled foraminiferal densities did not differ significantly. This differential response resulted in a change in the meiobenthic community structure which was apparent after 1 mo. The change is reflected, and can be followed, in the foraminifera:nematode ratio, which is proposed as a bio-indicator of prolonged anoxia. The results clearly demonstrate that, among the meiobenthos, hard-shelled foraminifera are most resistant to prolonged anoxia. However, conditions resulting from the anoxic treatment (e.g. decreased biological interactions) were beneficial to some foraminiferal genera. This resulted in a shift in faunal patterns eventually leading to a strong reduction in foraminiferal generic diversity. Results also indicated that details of these trends may not be evident if only the part of the foraminiferal assemblage retained on a 63 mu m sieve is examined.
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The distribution of modern symbiont-bearing larger foraminifera is confined to tropical and subtropical shallow water marine habitats and a narrow range of environmental variables (e.g. temperature). Most of today's taxa are restricted to tropical and subtropical regions (between 30°N and 30°S) and their minimum temperature limits are governed by the 14 to 20°C isotherms. However, during times of extensive global warming (e.g., the Eocene and Miocene), larger foraminifera have been found as far north as 50°N (North America and Central Europe) as well as towards 47°S in New Zealand. During the last century, sea surface temperatures have been rising significantly. This trend is expected to continue and climate change scenarios for 2050 suggest a further increase by 1 to 3°C. We applied Species Distribution Models to assess potential distribution range changes of three taxa of larger foraminifera under current and future climate. The studied foraminifera include Archaias angulatus, Calcarina spp., and Amphistegina spp., and represent taxa with regional, superregional and global distribution patterns. Under present environmental conditions, Amphistegina spp. shows the largest potential distribution, apparently due to its temperature tolerance. Both Archaias angulatus and Calcarina spp. display potential distributions that cover currently uninhabited regions. Under climate conditions expected for the year 2050, all taxa should display latitudinal range expansions between 1 to 2.5 degrees both north- and southward. The modeled range projections suggest that some larger foraminifera may colonize biogeographic regions that so far seemed unsuitable. Archaias angulatus and Calcarina spp. also show an increase in habitat suitability within their native occurrence ranges, suggesting that their tolerance for maximum temperatures has yet not been fully exploited and that they benefit from ocean warming. Our findings suggest an increased role of larger foraminifera as carbonate producers and reef framework builders in future oceans.
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Long-term observations on living benthic foraminifera in the laboratory were performed to investigate their behaviour and life style. We noticed that the formation of cysts or sedimentary envelopes is a common feature within many groups of foraminifera (organic walled, agglutinated and calcareous) in the laboratory. Several kinds of cyst were observed. In most cases, the entire foraminiferal shell was canopied with detritus or particles, but some specimens covered only parts of their body, such as the aperture region or pseudopods. Cysts were found attached to the glass walls of culture vessels or free in and on the sediment. Foraminifera stayed within cysts for hours to weeks. After leaving sedimentary envelopes, some specimens immediately started to build new ones, others not. The function of cyst formation observed in the present study was not clear, except one case where reproduction took place. Some monitored structures seemed not to be sedimentary cysts but unilocular agglutinated foraminifera with probably allogromiid-like organization. The formation of sedimentary envelopes seems to be a very basic character of foraminifera, suggesting a mechanism for the evolution of shells.
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We report on the survival and germination of up to a century-old marine protist resting stages naturally preserved in sediments from Koljö Fjord on the west coast of Sweden. This work has focused on germination of dinoflagellate cysts, but diatom resting stages were also observed. We record the longest known survival of dormant dinoflagellate cells. We individually isolated more than 1200 cysts of the three most abundant dinoflagellate taxa: Pentapharsodinium dalei, Lingulodinium polyedrum and Scrippsiella spp. Germination success decreased with core depth, and all successful germinations took place within the first 2 wk of incubation. Pentapharsodinium dalei had the highest germination success rate, with a maximum of up to 80% in 28-yr-old sediment, and could successfully germinate from core sediments dated to 1920 6 12. Scrippsiella spp. cysts with cell contents occurred down to c. 90-yr-old sediment and could germinate from down to ca. 40-yr-old sediments, with a maximum germination rate of 50–60% in recent sediments. Cysts of L. polyedrum germinated frequently down to 20 yr and rarely to c. 80 yr, with a maximum of 20–50% germination success in recent sediments. Cyst isolation under cooled conditions rather than at room temperature resulted in a significantly higher germination success in P. dalei, while no effect was observed for L. polyedrum. The time elapsed since slicing of the core affected survival of L. polyedrum cysts negatively, most likely due to the effect of oxygen. The long-term survival potential of benthic resting stages that we report here has important implications, as viable resting stages accumulated in bottom sediments can be transported back to the water column by, for example, bioturbation and human-mediated sediment dredging. Hence, the sediment may to a higher degree than previously considered play a role as seed bank. This is important in a changing climate and might have particularly severe impacts in the case of harmful species.
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ABSTRACT _______________________________________________________________ A new suprageneric system of the agglutinated foraminifera is offered consisting of five subclasses (Astrorhizana, Ammodiscana, Miliamminana (= Schlumbergerinana), Hormosinana, and Textulariana) belonging to five different classes, 27 orders, 156 families, 147 subfamilies, and 849 genera. The whole foraminiferal group is regarded as a phylum. The taxonomical significance of the different taxonomic features is discussed. In contrast to the majority of classification schemes adopted, the basic morphological characteristics of the test such as number of chambers (one, two or many), mode of coiling, test and chamber form, structure and position of the main and additional apertures, and the presence or absence of integrative systems are considered as having preferential significance compared with the character of the shell wall. The latter having important but subordinate value. The forms with different kinds of agglutinated wall are considered as ancestral stages in the evolutionary development of various phyletic lineages having different types of calcareous shell microstructure in their most advanced forms. Thus, the former Textulariacea are split into five groups according to their morphology. The taxonomic composition of each group elaborated up to the generic level is given as a preliminary scheme. Five new orders (Plagioraphida, Sphaeramminida Mikhalevich & Kaminski, Loftusiida Kaminski & Mikhalevich, Nautiloculinida, Verneuilinida Mikhalevich & Kaminski), five new families (Cystamminidae, Vaniidae, Reophacellidae Mikhalevich & Kaminski, Agglutisolenidae, Duotaxidae, Crenaverneuilinidae) and 15 new subfamilies (Praesphaerammininae Kaminski & Mikhalevich, this work, Ovammininae, Caudammininae, Agardhellinae, Reophacellinae Mikhalevich & Kaminski, Pseudoreophaxinae Mikhalevich & Kaminski (with the type species Pseudoreophax cisovnicensis Geroch, 1961, non Pseudoreophacinae Suleymanov, 1963 – invalid according to Loeblich & Tappan, 1987 (with type sp. Pseudoreophax marginulinae Suleymanov, 1963 (= Adelungia Suleymanov, 1966)), Vaniinae, Cylindroclavulininae, Trematophragmoidinae, Norvanganinae, Cribrobigenerininae, Voloshinovellinae, Cribrobulimininae, Goesellinae, Vacuovalvulininae) are described.
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In situ observations of microhabitat preferences of living benthic foraminifera are presented from sediments of the Norwegian-Greenland Sea, the upwelling area off northwestern Africa and the shallow-water Kiel Bight (Baltic Sea). Certain foraminiferai species (e.g. Cibicidoides wuellerstorfi and Rupertina stabilis) can be regarded as strictly epibenthic species, colonizing elevated habitats that are strongly affected by bottom water hydrodynamics. Large epibenthic forami-nifera (e.g. Rhabdammina abyssorum and Hyperammina crassatina) colonize the sediment surface in areas where strong bottom currents occur and might have by virtue of their own size an impact on the small-scale circulation patterns of the bottom water. Motile species changing from epifaunal to infaunal habitats (e.g. Pyrgo rotalaria, Melonis barleeanum, Elphidium excavatum clavatum, Elphidium incertum, Ammotium cassis and Sphaeroidina bulloides) are regarded here as highly adaptable to changes in food availability and/or changing environmental conditions. This flexible behaviour is regarded as a dynamic adaptation to optimize food acquisition, rather than a static concept leading to habitat classification of these ubiquitous rhizopods.
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The Ammonia-Elphidium foraminiferal index (A-E index) was first used in 1996 on the Louisiana inner continental shelf as a paleohypoxia tracer in the sedimentary record. This index, based on relative abundances of Ammonia and Elphidium (widespread and well-preserved taxa in coastal sediments), was considered a proxy for oxygen depletion because (1) Ammonia is more tolerant to prolonged oxygen depletion than Elphidium- and (2) the A-E index correlated well with organic carbon in surface sediment. A direct correlation between the A-E index and the level of bottom-water oxygen was found later in an independent study in Long Island Sound. Recent data generated by several workers confirm that the A-E index is a dependable tracer of historical paleohypoxia in coastal areas of rapid sedimentation. In cores taken from 10-30 rn depths in the nor-them Gulf of Mexico, the increasing trend of the A-E index reflects a worsening spring and summer oxygen stress over much of the 20(th) century. In Long Island Sound and Chesapeake Bay, the index traces an increase in hypoxia in water depths <25 m that began in the early 1970s. Overall, present data from the southeastern and eastern U.S. indicate that the A-E index is an excellent tracker of coastal paleohypoxia on a decadal scale (and, in exceptional cases, on an annual scale) when an undisturbed, continuous record of sedimentation is available, and when the effects of possible co-varying factors (e.g. salinity) are minimal.
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The measurement of species diversity represents a powerful tool for assessing the impacts of human activities on marine ecosystems. Traditionally, the impact of fish farming on the coastal environment is evaluated by monitoring the dynamics of macrobenthic infaunal populations. However, taxonomic sorting and morphology-based identification of the macrobenthos demands highly trained specialists and is extremely time-consuming and costly, making it unsuitable for large-scale biomonitoring efforts involving numerous samples. Here, we propose to alleviate this laborious task by developing protist metabarcoding tools based on next-generation sequencing (NGS) of environmental DNA and RNA extracted from sediment samples. In this study, we analysed the response of benthic foraminiferal communities to the variation of environmental gradients associated with salmon farms in Scotland. We investigated the foraminiferal diversity based on ribosomal minibarcode sequences generated by the Illumina NGS technology. We compared the molecular data with morphospecies counts and with environmental gradients, including distance to cages and redox used as a proxy for sediment oxygenation. Our study revealed high variations between foraminiferal communities collected in the vicinity of fish farms and at distant locations. We found evidence for species richness decrease in impacted sites, especially visible in the RNA data. We also detected some candidate bioindicator foraminiferal species. Based on this proof-of-concept study, we conclude that NGS metabarcoding using foraminifera and other protists has potential to become a new tool for surveying the impact of aquaculture and other industrial activities in the marine environment.This article is protected by copyright. All rights reserved.
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The limitations of a traditional morphology-based classification of Foraminifera have been demonstrated by molecular phylogenetic studies for several years now. Despite the accumulation of molecular data, no alternative higher-level taxonomic system incorporating these data has been proposed yet. Here, we present a new supraordinal classification of Foraminifera based on an updated SSU rDNA phylogeny completed with the description of major morphological trends in the evolution of this group. According to the new system, multi-chambered orders are grouped in two new classes: Tubothalamea and Globothalamea. Naked and single-chambered Foraminifera possessing agglutinated or organic-walled tests are arranged into a paraphyletic assemblage of “monothalamids”. The new system maintains some multi-chambered calcareous orders, such as Rotaliida, Miliolida, Robertinida and Spirillinida, although their definitions have been modified in some cases to include agglutinated taxa. The representatives of the planktonic order Globigerinida are tentatively included in the order Rotaliida. The agglutinated Textulariida are probably paraphyletic. The position of the order Lagenida is uncertain because reliable molecular data are only available for one species. The new classification system separates orders or families, which differ in basic chamber shapes, prevailing mode of coiling and distance between successive apertures. It appears that these features correspond better to the main evolutionary trends in Foraminifera than wall composition and structure, both used in traditional classification.
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Abstract While much evidence indicates that certain benthic foraminifera are facultative anaerobes, little is known regarding the physiologic response of foraminifera to anoxia. In order to assess their response, specimens of four foraminiferal species, collected from a typically dysoxic area of Drammensfjord, Norway (45 m water depth), were incubated in seawater purged with nitrogen. Over a time course of > 3 weeks, the specimens were extracted for adenosine triphosphate (ATT’) in a nitrogen-flushed glove bag to assess their survival and ATP reserve under such conditions. For comparative purposes, similar extractions were done on conspecifics one week after their collection from the seafloor, as well as on other conspecifics, obtained from the same site, incubated in aeratedconditions. The survival rates of nitrogen-treatedAdercotryma glomeratum, Psammosphueru bowmunni. and Stuinfi,rtlzia,f~s~~~rmis were not significantly lower than those of the control specimens. However, the ATP concentrations of nitrogen-incubated A. glomerutum and S. fisiformis were significantly lower than those of their aerated conspecifics, while there was no significant difference between,the [Al?] of P. bowmnnni,from,the two treatments. Both the survival rate and the ATP concentrations,of nitrogen-incubated,Bulimina,marginatu,were,significantly lower than those of control specimens.,The ultrastructure,of B. murginatu,and S.fis$“otmis incubated,in N2 for 18 days were compared,with those of specimens,fixed within I5 minutes of collection. For both species, the specimens that survived the experimental treatment had ultrastructures indistin- guishable from those fixed just after field collection. However, the ultrastructure of B. murginatu differed from that of S. .fir.sifi~rmi.s in that it lacked,the numerous,peroxisome-endoplasmic,reticulum,(ER) complexes,and what,appeared,to be algal chloroplasts,observed,in S. .fusiformis. Copious,arrays of paracrystals,were,observed,in both species from,the experimental treatment as well as the shipboard-fixed specimens, suggesting that neither population had extensive pseudopodial networks. When considered in combination, our results indicate that the four species respond to and survive anoxia differently, with responses including dormancy and, as yet unidentified, anaerobic metabolic pathways.
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Benthic foraminiferal and geochemical data from the Monte del Casino section in northern Italy are employed to reconstruct the sequence of events preceding the Late Miocene Mediterranean salinity crisis. We evaluate the effects of eustatic sea-level changes and tectonic events, affecting the Atlantic–Mediterranean connections. Changing benthic foraminiferal assemblages record changes in the deep-water environment, that can be explained by progressive isolation of the Mediterranean basin. The results of the analyses of stable oxygen- and carbon isotopes and redox-sensitive elements are in line with the benthic faunal trends. At 7.16 Ma, a first major step in isolation of the basin is indicated by the nearly simultaneous disappearance of a group of deeper-water benthic species usually found in middle to lower slope environments. At the same time, stable isotopes and redox-sensitive elements indicate cooling and decreasing bottom water oxygenation. After 6.8 Ma gradual development of water-mass stratification, probably accompanied by increasing bottom-water salinity, is indicated by all proxies. The cyclic pattern of homogeneous and sapropelitic sediments in the section is related to astronomical parameters, and allows a detailed correlation with Mediterranean sections at considerable geographic distances. We compared the benthic foraminiferal faunas with those from the Metochia section (Gavdos, Greece), deposited at a similar water depth (∼1000 m), to find that the benthic foraminifera at both sites indicate a similar, synchronous paleoenvironmental development. All proxies indicate that the onset of the Late Miocene Mediterranean salinity crisis dates back to the earliest Messinian. The development of the Mediterranean basin toward an evaporite trap is a result of interactions between a 400-kyr eccentricity related climatic effect superimposed upon gateway dynamics at the Atlantic–Mediterranean connections. Benthic foraminifera accurately record the steps in increasing isolation of the Mediterranean basin.
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The numbers of benthic foraminiferans at four sites in the Clyde Sea area showed no consistent temporal variation throughout 1993. In the finest surface sediments, numbers ranged between 200 and 400 cellscm−3, compared to only 25–50 cellscm−3in the coarsest sediments. On two occasions, high populations of cells less than 63μm were found in the surface layers. These were thought to represent recruitment peaks since these ‘juvenile’ cells grew rapidly when maintained in the laboratory. A total of 56 taxa were identified from the region, the greatest diversity being recorded in the finest sediments. Rose Bengal stained foraminiferans (i.e. presumed living) were found below the anoxic–oxic boundary. The fate of these cells was considered by examining their ability to migrate through fine sediments, and their capacity to survive (based on evidence of pseudopodial activity) periods of anoxia. This study has highlighted the numerical importance of foraminiferans, particularly in fine surface coastal sediments, but questions whether the high populations of ‘stained’ cells found in deeper sediments play a significant ecological role.
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The deep ocean environment is disturbed by various processes, many of which involve episodic inputs of organic matter. Some inputs (e.g., phytodetritus at mid-high latitudes in the North Atlantic and Northeast Pacific) are seasonally pulsed, others (e.g., falls of whale carcasses) are irregular and unpredictable, but together, they evoke a variety of responses from the benthic biota. In the case of deep-sea foraminifera, only those responses arising from seasonal food pulses have been fairly well-documented. The population dynamics of deep-sea benthic foraminifera (total live populations and individual species) appear to be controlled largely by two inversely-related parameters, the flux of organic matter to the seafloor and concentrations of oxygen in the sediment porewater. Organic matter (food) inputs are most intense along bathyal continental margins, and their oxidation often leads to the depletion of oxygen in surface sediments. Under these conditions, foraminiferal faunas are dominated by low-oxygen tolerant, infaunal species, the abundance of which fluctuate in response to seasonally varying amounts of food and oxygen. At some sites (e.g., Sagami Bay, off Japan), species migrate up and down in the sediments, tracking critical oxygen concentrations. Where oxygen concentrations are consistently low (less than about 0.5 ml l−1), as in parts of the California Borderland, foraminifera may undergo population increases solely in response to food pulses. In the abyssal North Atlantic, and in some continental margin areas of this ocean, organic matter inputs are weaker and do not lead to oxygen depletion within surface sediments. These systems are food limited and seasonal population fluctuations reflect the availability of food (phytodetritus) rather than oxygen. Here, the species which respond to phytodetritus are mainly epifaunal or shallow infaunal opportunists which represent a small proportion of highly diverse communities (2 or 3 out of >120 species per core of 25.5 cm2 surface area). Seasonal phytodetrital pulses to the deep-seafloor, and hence, foraminiferal population dynamics, are not entirely predictable. Being dependent on climatic and upper-ocean processes, they vary in intensity from year to year and occasionally (e.g., at the Porcupine Abyssal Plain (PAP) in 1997) fail to materialise. Foraminiferal responses to irregular (non-seasonal) organic matter inputs are poorly-known. However, there is some evidence that whale falls, turbidite deposits, hydrothermal vents and seeps are exploited by species typical of organically-enriched, low-oxygen environments rather than by a specialised fauna.Fossil foraminiferal assemblages from bathyal and abyssal environments may provide evidence for an increase or decrease in the seasonality of surface production as well as for longer-term changes in palaeoproductivity. However, the accurate interpretation of this record depends on filling the many gaps which remain in our understanding of relations between benthic foraminiferal ecology and seasonal phenomena in the deep ocean.
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Variations in oceanic primary productivity, flux of organic carbon to the sediments, and dissolved-oxygen levels in the water column are thought to be important in the control of benthic foraminiferal test size, wall thickness, morphology, and species composition of assemblages by many foraminiferal paleontologists. Aspects of these processes should be reflected by the benthic foraminiferal oxygen index (BFOI) based on these foraminiferal characteristics. However, analyses indicate that the BFOI correlates most strongly with dissolved-oxygen levels in overlying water (R2=0.81), weakly with oceanic primary productivity (R2=0.55), and weakly with organic carbon flux to the sediments (R2=0.51). Although both dissolved oxygen and organic carbon flux are main controlling factors for benthic foraminiferal assemblages, the BFOI is a useful indicator extracted from benthic foraminiferal assemblages for estimating the condition of dissolved oxygen in Cretaceous and Cenozoic oceans.
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The eight previous Leeuwenhoek Lectures covered a great variety of problems is bacteriology and virology, and each of the lecturers paid an enthusiastic tribute Antony van Leeuwenhoek as the founder of microbiology. When the Council honoured me by their invitation to deliver the ninth Leeuwen hoek Lecture I thought that it would be appropriate to devote it to the problem of anabiosis or latent life.
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The top 4 cm c: replicate core samples from near the entrance to the West Passage of Narragansett Bay, Rhode Island, taken in 1963 were individually examined; presumed living and dead specimens were found at all four levels. Data on over 5,000 living and 7,500 dead specimens were collected from 283 samples. The use of a two-stage s'ampling technique for determination of an optimum number of samples is described. The frequency distributions of the numbers of both presumed living and dead A. beccarii could bc normalized successfully with a log (X + 1) trans- formation. At each of the four levels, the numbers of both living and dead individuals rcmaincd statistically constant, and the number of prcsumcd living A. beccurii was the same in the three top l-cm levels but significantly greater there than at the fourth, while there wcrc significantly fewer dead specimens in the first centimeter than in the third and fourth,
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We investigated the distribution of living (stained) benthic foraminifera across a tropical, intertidal shoreline adjacent to Cocoa Creek, Queensland, Australia for the purpose of better understanding the nature of test production and ultimately fossil assemblage development within such environments. Short cores (up to 1 m) were collected during the wet and dry season, along an elevational gradient comprising non-vegetated intertidal mudflat and higher-intertidal mangrove forest environments. The distribution of stained specimens can be broadly delineated into assemblages characterising ‘upper mangrove’ (2.64–2.91 m above Lowest Astronomical Tide (LAT)) and ‘low mangrove-mudflat’ (1.62–2.18 m above LAT) environments. Agglutinated species were generally limited to upper mangrove stations. Calcareous species occurred within all of the intertidal environments examined but differ in their composition between upper and lower intertidal settings. Upper mangrove faunas were characterised by the agglutinated species Arenoparrella mexicana, Haplophragmoides wilberti, Miliammina fusca, Miliammina obliqua and Trochammina inflata and the calcareous species Helenina anderseni. Live (stained) assemblages at lower intertidal elevations were dominated by the calcareous species Ammonia aoteana, as well as Rosalina spp., Elphidium oceanicum, Triloculina oblonga, Ammonia pustulosa and Shackoinella globosa.
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The foraminiferan Glabratella ornatissima (Cushman) dominates the shallow turbulent coastal zone from central California to the Arctic Ocean. The species was sampled weekly for 2yr near the Bodega Marine Laboratory, 50mi N of San Francisco, California, at a depth of 3.2m below mean low water. Rapid growth, reproduction and a complex alternation of generations are related to abundant food supply due to seasonal upwelling, increased wave action, and sediment transport.-from Authors