Paleobiology (2018) 44 (3): 460-489.
We report a detailed study of the different categories and types of abnormal morphologies in planktic foraminifera recognizable in the lowermost Danian, mainly from the El Kef and Aïn Settara sections, Tunisia. Various types of abnormalities in the test morphology were identified, including protuberances near the proloculus, abnormal chambers, double or twinned ultimate chambers, multiple ultimate chambers, abnormal apertures, distortion in test coiling, morphologically abnormal tests, attached twins or double tests, and general monstrosities. Detailed biostratigraphic and quantitative studies of the Tunisian sections documented a major proliferation of aberrant planktic foraminifera (between approximately 5% and 18% in relative abundance) during the first 200 Kyr of the Danian, starting immediately after the Cretaceous/Paleogene (K/Pg) boundary mass extinction (spanning from the Guembelitria cretacea Zone to the lower part of the P. pseudobulloides Zone). This contrasts with the proportionately low frequency of aberrant tests (generally <2%) identified within the uppermost Maastrichtian, suggesting more stable environmental conditions during the last ~50–100 Kyr of the Cretaceous. Two main pulses with abundant aberrant tests were recognized in the earliest Danian, the one recorded in the well-known K/Pg boundary clay being the more intense of those (maxima of >18%). These main pulses of aberrants coincide approximately with relevant quantitative and evolutionary turnovers in the planktic foraminiferal assemblages. In this paper, we explore the relation of these high values of the foraminiferal abnormality index with the environmental changes induced by the meteorite impact of Chicxulub in Yucatan, Mexico, and the massive eruptions of the Deccan Traps, India.
Asteroid impacts represent an extreme among natural disasters, inducing rapid and sharp environmental perturbations with important implications for the biosphere (Alvarez et al. 1992; Toon et al. 1997). After the Chicxulub asteroid impact (Yucatan, Mexico) at the Cretaceous/Paleogene (K/Pg) boundary (Hildebrand et al. 1991), a cloud of dust and fine ejecta scattered and contaminated the atmosphere, land, and oceans (Alvarez et al. 1980; Smit and Hertogen 1980). The cloud of pulverized impact material at Chicxulub was deposited slowly (probably over a few years), forming a thin (few millimeters) airfall layer evident in deep-marine sediments worldwide, with anomalous concentrations of iridium and other platinum-group metals, nickel-rich spinels, shocked quartz, and altered microtektites (Smit 1990; Robin et al. 1991). The Chicxulub impact caused the blockage of sunlight, the inhibition of the photosynthesis, disruption of food chains, a sudden drop in global temperature, destruction of the ozone layer, and the production of toxins and acid rain (Smit and Romein 1985; Hsü and McKenzie 1985; Pope et al. 1997; Gerasimov 2002; Ocampo et al. 2006; Alegret et al. 2012; Bardeen et al. 2017), initiating one of the greatest mass extinctions in the history of life (Schulte et al. 2010).
In the earliest Danian oceans, a dark-clay bed was deposited above the K/Pg airfall layer under conditions of global climatic warming and alterations in oceanic productivity (Hsü and McKenzie 1985; D'Hondt et al. 1998; D'Hondt 2005; Coxall et al. 2006; Birch et al. 2016), with some regions showing a sharp decline in export productivity during approximately 2 Myr, and others a constant or rapidly reestablished organic flux from the surface ocean to the deep seafloor (Hull and Norris 2011).
The dark-clay bed also contains high concentrations of heavy metals, which, though lower than in the airfall layer, are higher than in the sediments of the upper Maastrichtian and more modern lower Danian (Smit and ten Kate 1982; Dupuis et al. 2001; Hollis et al. 2003). The paleoenvironmental conditions recorded in the dark-clay bed seem therefore to reflect the long-term disruptive effects of the K/Pg impact event, revealing a time in which the ecosystems were starting to recover and oceanic productivity to re-establish itself.
Planktic foraminifera, like other paleontological groups, suffered considerable, but not complete, extinction at the K/Pg boundary event (Smit 1982). The cause–effect relationship between the Chicxulub impact and the K/Pg mass extinction has been amply verified (see Smit 1990, 1999; Arenillas et al. 2000b, 2006), and the impact theory is correspondingly well established in the scientific community (Schulte et al. 2010). However, other evidence seems to suggest that the massive eruptions of the Deccan Traps, India, could have played an important role in the extinction, or at least in the paleoenvironmental changes that occurred during the Cretaceous/Paleogene transition (Courtillot et al. 1988; Chenet et al. 2007, 2009; Keller et al. 2011, among others). Recently, Schoene et al. (2015) has applied uranium-lead (U-Pb) zircon geochronology to Deccan rocks, showing three main eruptive phases or megapulses, the main one (phase 2) beginning approximately 250 Kyr before K/Pg boundary and lasting 750 Kyr.
The Deccan megapulses have been related to episodes of global warming and/or environmental stress across the K/Pg boundary (Keller and Pardo 2004; Pardo and Keller 2008; Punekar et al. 2014, 2016). Keller et al. (2011) proposed that phase 2 (responsible for ca. 80% of the total volume of Deccan Traps emissions) ended at or near the K/Pg boundary, spanning the last 280 Kyr of the Maastrichtian. Deccan-induced global warming and cooling episodes at the late Maastrichtian seem to be responsible for dwarfing episodes in some planktic foraminiferal species (Keller and Abramovich 2009; Omaña et al. 2012; Petersen et al. 2016), migrations (Olsson et al. 2001), and regional assemblage changes (Keller 2003), however, without a significant decrease in global planktic foraminiferal diversity (Arenillas et al. 2000a,b). After the K/Pg boundary, small species began to appear following a model of "explosive" adaptive radiation (Smit 1982; Brinkhuis and Zachariasse 1988; Arenillas et al. 2002, 2004). One of the ancestors of the first Danian species was the opportunistic, triserial genus Guembelitria, which might be the only true survivor (Smit 1982, 2004). However, the main lineages of planktic foraminifers appearing in the Danian, whose descendants have reached the present day, could have a benthic origin (see Brinkhuis and Zachariasse 1988; Arenillas and Arz 2017). It must be emphasized that there are other relevant taxonomic and phylogenetic models, some of them highly supported among planktic foraminifer taxonomists. Among the most noteworthy proposals are those of Olsson et al. (1999), Apellaniz et al. (2002), Aze et al. (2011), and Koutsoukos (2014), which suggest that the genus Muricohedbergella was a survivor of the K/Pg extinction event and played an important phylogeny role for being the ancestral form of Danian genera such as Globanomalina, Eoglobigerina, and/or Praemurica.
Abnormal tests have long been reported in recent benthic foraminifera linked to regions with either high environmental variability (e.g., Polovodova and Schonfeld 2008; Ballent and Carignano 2008) or human-induced pollution (e.g., Yanko et al. 1998; Samir and El Din 2001; Frontalini and Coccioni 2008), showing that abnormal variations in morphology are a response to changes in ecological parameters such as temperature, pollution, carbonate solubility, dissolved oxygen, or the occurrence of rapid environmental fluctuations. The long-term effects of Chicxulub impact and the Deccan eruptions probably triggered similar ecological stress conditions, thus inducing similar malformations in planktic foraminiferal tests. Indeed, abnormal planktic foraminifers have been reported right above the K/Pg boundary, mainly in Guembelitria (Coccioni and Luciani 2006). Similar increases in abnormal planktic tests have been observed in warming episodes and episodes of ecological stress, such as the Cretaceous ocean anoxic events (Verga and Premoli Silva 2002) or the Paleocene–Eocene Thermal Maximum (Luciani et al. 2007). However, studies on the aberrant planktic foraminifers of the K/Pg transition from a taxonomic and paleoenvironmental point of view are still very limited and fragmented.
Abnormalities are formed when the ontogenetic plan of the test is disrupted and this disruption generates an irregular shape in comparison with other specimens of the same species (Murray 2006). In recent foraminifera, abnormalities produced during the life and growth of an individual may be due either to mechanical or ecological causes (Boltovskoy and Wright 1976; Murray 2006). In the case of planktic foraminifera, the causes behind test abnormalities may be predation breakages, but abnormal planktic specimens seem to reflect mainly stressful environmental conditions (Montgomery, 1990; Luciani et al. 2007). In addition, abnormalities can also be produced by mutations. The phenotypic consequences of mutations can vary, but in the case of fossil foraminifera, the most interesting ones are those that affect the test morphology. Mutations can cause lethal or physiologically nonfeasible aberrations, but could have also generated new species, probably bringing on the early Danian evolutionary radiation mentioned earlier (BouDagher-Fadel 2012; Arenillas et al. 2016).
In this paper, a wide variety of morphological abnormalities in planktic foraminiferal tests from the earliest Danian are described for the first time, mainly from Tunisian sections. We use a quantitative approach to identify changes in the abundance of aberrant tests and correlate them with evolutionary radiations and other shifts recognized in the planktic foraminiferal assemblages across the K/Pg boundary. The main aim is to inquire into the causes that could have triggered the proliferation of aberrant tests before and after the K/Pg boundary mass extinction, and the relation of these causes with the environmental changes induced by the Deccan eruptions and the Chicxulub impact.
We studied samples from localities considered to be the most expanded and continuous marine K/Pg sections worldwide, such as El Kef, Aïn Settara, and Elles (Tunisia), and Agost and Caravaca (Spain). The El Kef section was chosen to define the Global Boundary Stratotype Section and Point (GSSP) for the base of the Danian stage, or the K/Pg boundary (Molina et al. 2006), while Caravaca, Elles, and Aïn Settara were chosen as auxiliary sections of the GSSP (Molina et al. 2009). The K/Pg boundary is defined at the base of the bed informally known as the "K/Pg boundary clay," specifically at the base of the 2- to 5-mm-thick airfall layer with high concentrations of iridium that coincides with the planktic foraminiferal extinction horizon (Smit 1990, 1999). The dark-clay bed overlying the K/Pg airfall layer is approximately 100 cm thick in El Kef, with a 50-cm-thick blackish clay overlain by a 50-cm-thick dark gray clay; it continues with 1-m-thick darkened gray marly clay and 60-cm-thick clayey marl, so the dark-clay bed thickness could be 200 cm or more in El Kef. It is characterized by low values of δ13C and CaCO3 content and high total organic carbon (TOC) values (Keller and Lindinger 1989). In Aïn Settara, the airfall layer is 5 to 10 mm thick, and the dark-clay bed is approximately 50 cm thick; this is also characterized by low values of δ13C and in CaCO3 content and high TOC values (Dupuis et al. 2001).
For the taxonomic studies, specimens were picked mainly from El Kef and Aïn Settara, where the foraminiferal test preservation is good (excellent at some samples), although specimens from other sections (Elles, Agost, and Caravaca) were used with the aim of conveniently illustrating some of the species and types of normal and abnormal growth morphologies identified in the lower Danian. Specimens considered to be normal forms are those that conform to some type of shape within the theoretical three-dimensional morphospace of serial and spiral foraminifeal tests proposed by Tyszka (2006). Taxonomic remarks and a systematic scheme for the normal forms of early Danian planktic foraminiferal species are provided in Supplementary Appendix A and Supplementary Figure 1.
All rock samples studied were disaggregated in water with diluted H2O2, washed through a 63 μm sieve, and then oven-dried at 50°C. The quantitative analyses were based on representative splits (using a modified Otto microsplitter) of approximately 300 specimens per sample, quantifying the relative abundance of both normal and abnormal tests in each group of planktic foraminifera (Tables 1, 2). For the quantitative study, we restudied 39 samples from El Kef and 35 samples from Aïn Settara (see Arenillas et al. 2000a,b). The specimens analyzed were mounted on microslides for a permanent record and identification. Planktic foraminifera were picked from the residues and selected for scanning electron microscopy (SEM), using the JEOL JSM 6400 and Zeiss MERLIN FE-SEM of the Electron Microscopy Service of the Universidad de Zaragoza (Spain). SEM photographs of the species considered here are provided in Supplementary Figures 2 and 3. For the illustration of these species, we used, in addition to El Kef and Aïn Settara, other localities characterized by the good preservation of their foraminiferal tests, such as Ben Gurion (Israel), Deep Sea Drilling Project (DSDP) Site 305 (North Pacific), and Bajada del Jagüel (Argentina).
For the Maastrichtian, the biostratigraphic and quantitative study focused mainly on the Plummerita hantkeninoides Subzone, which spans the last 140 Kyr of the Cretaceous according to Husson et al. (2014). This biozone is defined by the total range of the nominate taxon and is equivalent to the alphanumeric Zone CF1 of Li and Keller (1998). For the lower Danian, we used the biozonation of Arenillas et al. (2004), and compared it with those of Li and Keller (1998) and Berggren and Pearson (2005) (the latter recently revised by Wade et al. 2011). Their equivalences are shown in Figure 1. The former is based on continuous, complete, and very expanded Tunisian and Spanish K/Pg sections such as El Kef, Aïn Settara, Elles, Caravaca, Agost, and Zumaia. It includes six subbiozones: the Muricohedbergella holmdelensis and Parvularugoglobigerina longiapertura Subzones of the Guembelitria cretacea Zone, the Parvularugoglobigerina sabina and Eoglobigerina simplicissima Subzones of the Pv. eugubina Zone, and the Eoglobigerina trivialis and Subbotina triloculinoides Subzones of the P. pseudobulloides Zone. The species ranges illustrated in Figure 1 are based on the stratigraphic distributions verified mainly in the El Kef stratotypic section. Note that the Mh. holmdelensis Subzone is equivalent to Zone P0 of Li and Keller (1998) and Berggren and Pearson (2005), whereas Zone Pα (or P1a of Li and Keller 1998) spans approximately the Pv. longiapertura, Pv. sabina, and E. simplicissima Subzones.
Arenillas et al. (2004) calibrated numerical ages of the biozonal boundaries on the basis of biostratigraphic and magnetostratigraphic data from Agost, Spain, and the timescale of Röhl et al. (2001), who astronomically calibrated the C29r/C29n reversal at 255 Kyr after the K/Pg boundary. Subsequent radiometric, paleomagnetic, and astronomical dating/calibrations have given different results for the age of the K/Pg boundary as well as the duration of the magnetozones. Taking into account the Geologic Time Scale 2012 (GTS12; Gradstein et al. 2012), which gives an age for the C29r/C29n boundary of 352 Kyr after the K/Pg boundary, the Mh. holmdelensis Subzone would span the first 7 Kyr after the K/Pg boundary, the Pv. longiapertura Subzone from 7 to 25 Kyr, the Pv. sabina Subzone from 25 to 46 Kyr, the E. simplicissima Subzone from 46 to 79 Kyr, the E. trivialis Subzone from 79 to 282 Kyr, and the S. triloculinoides Subzone from 282 to 616 Kyr.
High-resolution quantitative studies of Tethyan sections make it possible to recognize three planktic foraminiferal acme-stages (PFAS) of high biochronological interest across the lowermost Danian in pelagic (oceanic and outer neritic) environments (see Arenillas et al. 2006): PFAS-1, dominated by the triserial Guembelitria; PFAS-2, dominated by tiny trochospiral, informally denominated parvularugoglobigerinids (Parvularugoglobigerina and Palaeoglobigerina); and PFAS-3, dominated by biserial Woodringina and Chiloguembelina. Following the GTS12, PFAS-1 would span the first 18 Kyr after the K/Pg boundary, PFAS-2 approximately from 18 to 62 Kyr, and PFAS-3 from 62 Kyr on. A second acme of triserials is identified in the lower part of PFAS-3, that is, in the transition between the Pv. eugubina and P. pseudobulloides Zones (Arenillas et al. 2017). This acme has been attributed to the genus Chiloguembelitria Hofker, 1978, not Guembelitria, and spans approximately from 70 to 200 Kyr according to the GTS12.
Many new species of trochospiral and biserial planktic foraminifers originated after the K/Pg boundary, as is shown in Figure 1 and described in Supplementary Appendix A. The systematic scheme in Supplementary Figure 1 is a good reflection of the morphological and textural diversity that appeared after the extinction event. As illustrated in Figure 1, the planktic foraminifera evolutionary radiation of the early Danian happened in two pulses (see also Arenillas et al. 2000a,b, 2017; Arenillas and Arz 2017). The first occurred between approximately 5 and 26 Kyr after the K/Pg boundary according to the GTS12, with the appearance of tiny, trochospiral species belonging to the parvularugoglobigerinids (Pseudocaucasina, Palaeoglobigerina, and Parvularugoglobigerina) and biserial taxa (Woodringina and Chiloguembelina), as well as triserial species of the genus Chiloguembelitria (Supplementary Figs. 1 and 2). The second evolutionary radiation occurred between approximately 46 and 110 Kyr after the K/Pg boundary according to the GTS12, giving rise to more ornamented, larger trochospiral species (Supplementary Figs. 1, 3) belonging to Trochoguembelitria, Eoglobigerina, Parasubbotina, Globanomalina, and Praemurica. Other genera appear shortly afterward, such as Subbotina and Globoconusa.
In the present work, the extinction and evolution of planktic foraminifers across the K/Pg boundary at the El Kef section were quantified using the evolutionary model proposed by Dean and McKinney (2001), which measures taxonomic turnovers using four metrics (Fig. 2): extinction rate (ER), speciation rate (NR), volatility (V), and taxonomic flux (F). Taxonomic flux F is used to estimate whether there are relative increases (positive values) or declines (negative values) in diversity. The volatility V indicates whether there is evolutionary stability (low values) or increased taxonomic turnover (high values). The method developed by Dean and McKinney (2001), which is described in Supplementary Appendix B, was applied to the stratigraphic ranges of planktic foraminiferal species recognized in the El Kef section (Supplementary Fig. 4). The present quantification of the evolutionary pattern is an update of the one already made at El Kef by Arenillas et al. (2002), taking into account the taxonomic and biostratigraphic revisions made since then (see Supplementary Appendix A). The metrics were measured under two alternative hypotheses, as already proposed by Arenillas et al. (2002): (1) all 16 Cretaceous species identified in lower Danian levels are in situ (pattern A in Supplementary Table 1): Muricohedbergella holmdelensis, Muricohedbergella monmouthensis, Heterohelix globulosa, Heterohelix planata, Heterohelix navarroensis, Heterohelix labellosa, Laeviheterohelix pulchra, Laeviheterohelix glabrans, Pseudoguembelina kempensis, Pseudoguembelina costulata, Globigerinelloides volutus, Globigerinelloides praeriehillensis, Globigerinelloides yaucoensis, Guembelitria dammula, Guembelitria cretacea, and Guembelitria blowi (see Supplementary Fig. 4); and (2) except for two Guembelitria species (Guembelitria cretacea and Guembelitria blowi), all Cretaceous species identified in lower Danian levels are reworked (pattern B in Supplementary Table 2).
According to these metrics, in both hypotheses (Fig. 2), four main evolutionary episodes were recognized: (1) an extremely high extinction rate coinciding with the catastrophic mass extinction at the K/Pg boundary; (2) a high speciation rate in the Pv. longiapertura Subzone coinciding with the first Danian evolutionary radiation, mainly of parvularugoglobigerinids; (3) a relatively high speciation rate in the E. simplicissima Subzone coinciding with the beginning of the second evolutionary radiation; and (4) a relatively high extinction rate in the basal part of the E. trivialis Subzone coinciding with the parvularugoglobigerinid extinction. Due to these evolutionary episodes, volatility is high at El Kef during approximately the first 200 Kyr of the Danian, which is also reflected by relevant fluctuations in the taxonomic flux. These data contrast with the extremely low volatility in the P. hantkeninoides Subzone of the uppermost Maastrichtian (Fig. 2).
Our quantitative study of planktic foraminifers has revealed a strong proliferation of aberrant forms above the K/Pg boundary in the El Kef and Aïn Settara sections (Fig. 3). At El Kef, the abundance of aberrant tests (Foraminiferal Abnormality Index, or FAI) in PFAS-1 is as high as 18.7% of the total population of planktic foraminifera, of which almost 90% are abnormal forms of the triserial Guembelitria. At Aïn Settara, the abundance of aberrant forms in PFAS-1 reaches over 12%, of which almost 70% are aberrant tests belonging to Guembelitria. These data contrast with the total percentage of aberrant tests in studied Maastrichtian samples (Tables 1, 2), which almost never exceeds 2.5% in either section (except for the basal part of the Aïn Settara section, whose FAI is as high as 3.4–3.6%). These include a few aberrant specimens, mainly of Heterohelix and Pseudoguembelina.
These percentages increase if we assume that the Maastrichtian specimens found in Danian horizons are reworked (pattern B hypothesis), except for two Guembelitria species (curves with black shading in Fig. 3). In this case, the FAI in PFAS-1 reaches almost 20% in El Kef and 18% in Aïn Settara. It should be noted that, except for Guembelitria, the percentages of other aberrant Maastrichtian specimens in the Danian are similar to those estimated for Maastrichtian horizons (Tables 1, 2), in contrast with the strong increase in aberrant tests among the Danian Guembelitria specimens within the dark-clay bed. This suggests that all these Maastrichtian specimens (aberrants and non-aberrants alike) are in fact reworked. A high-resolution biostratigraphic analysis at the Moncada section, Cuba, revealed that, with the exception of Guembelitria species, there were no cosmopolitan, generalist Cretaceous species in the lowermost Danian deposits, not even in Zone P0 and the dark-clay bed (Arenillas et al. 2016). This evidence led the authors to suggest that the planktic foraminiferal mass extinction at the K/Pg boundary was more severe and catastrophic than previously suggested and that the presence of Cretaceous species within the lowermost Danian deposits at most K/Pg localities may be the result of normal reworking/bioturbation processes worldwide (see also Huber 1996; Kaiho and Lamolda 1999; Huber et al. 2002). In any case, whether we consider the pattern A hypothesis or that of pattern B, the abundance curves indicate similar trends (Fig. 3).
Aberrant Guembelitria specimens have frequently been classified as Guembelitria irregularis (e.g., Coccioni and Luciani 2006). This species has no doubt been used as a "wastebasket" taxon that also includes the aberrant forms of both Maastrichtian and Danian guembelitriids (see discussion in Arz et al. 2010). However, we consider here that irregularis is a genuine Danian species, including normal triserial forms (see Supplementary Fig. 1), because the abnormal morphologies among guembelitriids are of another kind. Arenillas et al. (2017) attributed irregularis to the genus Chiloguembelitria instead of Guembelitria, on the basis of differences in the wall texture and position of the aperture. Chiloguembelitria irregularis groups Danian specimens with twisted triserial arrangements of irregular appearance, corresponding to the irregular morphophase of the model of Tyszka (2006). Nevertheless, if these specimens are also counted as abnormal forms, then the FAI during the earliest Danian is even more anomalous, reaching more than 23% in PFAS-1 at El Kef, according to the pattern B hypothesis (Fig. 3).
During the episode PFAS-1, abnormalities are frequent in all planktic foraminiferal groups, suggesting that ecological stress affected all pelagic environments during the early Danian. The FAI in the upper PFAS-1 is high not only in guembelitriids but also in parvularugoglobigerinids; for example, almost 40% of parvularugoglobigerinid specimens from the sample at 97 cm above the K/Pg boundary at El Kef have some type of abnormality. Subsequently, the abundance of aberrant tests decreases during PFAS-2 but remains relatively high in both El Kef and Aïn Settara, at around 3–10% (in both patterns A and B), suggesting that the environmental conditions remained unstable tens of thousands of years after the K/Pg boundary. Another increase in the FAI has been recognized across the boundary between the Pv. eugubina and P. pseudobulloides Zones (mainly in the E. trivialis Subzone, or Subzone P1a), rising to a maximum of 11% (in both patterns A and B) in El Kef and Aïn Settara (Fig. 3). The increase in aberrant forms is more evident among triserial and biserial specimens of the genera Chiloguembelitria, Woodringina, and Chiloguembelina. This interval coincides with the second bloom of triserials in the lower part of PFAS-3 (Fig. 3), in this case caused by Chiloguembelitria and not by Guembelitria. Guembelitria comprised opportunistic species whose relative abundance strongly increased in ecological stress conditions, mainly related to eutrophication episodes (see e.g., Keller and Pardo 2004). Chiloguembelitria replaced Guembelitria in the early Danian, occupying a similar ecological niche (Arenillas et al. 2017), so its blooms indicate similar conditions of ecological stress. Maxima in aberrant specimens thus seem to coincide with guembelitriid blooms in the early Danian, as occurs in PFAS-1 and the lower part of PFAS-3.
Various types of abnormalities are present among the earliest Danian planktic foraminifers, severely complicating their taxonomic identification in some cases. Abnormal specimens have previously been reported in the lowermost Danian of other localities, mainly among Guembelitria (Coccioni and Luciani 2006) but also among parvularugoglobigerinids (Gerstel et al. 1986). Double and multiple tests of Parasubbotina and Globoconusa were also described by Ballent and Carignano (2008) in shallow environments of the Cerro Azul section, Argentina.
Protuberance near the proloculus, which includes two types: (a) protruding proloculus (Fig. 4A1); and (b) second chamber abnormally protruding beside the proloculus (Fig. 4A2), also known as a double- or twinned-chamber arrangement. The latter occurs during the calcification of juvenile individuals and may be a result of frustrated double tests (Stouff et al. 1999). During the early ontogenetic stage, two chambers can grow from the proloculus with subsequent development of an independent whorl from each of the second chambers; if a single whorl develops from one of these chambers, then the other appears as a protuberance on the proloculus (Polovodova and Schönfeld 2008).
Chamber abnormalities, which include six types: (a) aberrant shapes (Fig. 4B1); (b) reduced chamber sizes (Fig. 4B2); (c) overdeveloped chambers of the last whorl (Fig. 4B3); (d) additional chambers (Fig. 4B4); (e) protuberant chambers (Fig. 4B5); and (d) welded chambers (Fig. 4B6). Overdeveloped and reduced chambers have been related to environmental stress (Hecht and Savin 1972). For benthic foraminifera, Sujata et al. (2011) proposed that abnormal chambers are a result of specimens being subjected to temporary hyposaline conditions, which causes considerable dissolution and the subsequent regeneration of the chamber in an abnormal form. The same phenomenon could be applied to planktic foraminifera in conditions of acidified waters with increased carbonate dissolution, as occur in global warming–hyperthermal episodes (e.g., Luciani et al. 2007).
Abnormal ultimate chamber, which includes five types: (a) aberrant shape (Fig. 4C1); (b) kummerform, or reduced last chamber (Fig. 4C2); (c) overdeveloped or inflated last chamber (Fig. 4C3); (d) anomalous position (Fig. 4C4) causing, for example, the change from biserial/triserial to uniserial; and (e) bulla-like chamber (Fig. 4C5), that is, the last chamber partially or totally covering the umbilicus, resembling a bulla. The first three types are identified here in all the planktic foraminiferal groups and are frequently associated with a decrease in ornamentation. The bulla-like last chamber is typical of high trochospiral specimens with an intraumbilical or quasi-intraumbilical aperture, as in some species of Palaeoglobigerina and Parvularugoglobigerina. Hecht and Savin (1972) reported that bulla-like abnormal chambers are more common in warmer waters and seem to develop on unusually long-lived specimens (Montgomery 1990). According to Bijma et al. (1992), abnormal last chambers could be induced by the ocean oxygen level, light quality, or feeding rate. Saclike overdeveloped chambers seem currently to be more common in upwelling areas characterized by waters that are more anoxic and richer in nutrients and in more yellow-green light conditions. Kummerform chambers are probably the result of the opposite conditions, that is, more oxygenated waters, oligotrophy, and light conditions (blue) typical of the open ocean.
Multiple ultimate chambers, which include two types: (a) double or twinned ultimate chambers (Fig. 4D1); and (b) proliferation of chambers in the last whorl(s) (Fig. 4D2). They are present mostly in triserial species (Guembelitria), but are also found here in the trochospiral Palaeoglobigerina. In Guembelitria, these additional chambers are usually disposed in several directions (multiserial forms). Many triserial specimens exhibit an ultimate tetraserial stage and have probably been misidentified as Palaeoglobigerina alticonusa and/or Trochoguembelitria alabamensis (see Supplementary Fig. 1). Others, mainly biserials, have two complete and identical ultimate chambers. According to Venturati (2006), twinned or bilobated chambers may be used as potential proxies for environmental stress. Montgomery (1990) suggested that specimens with multiple last chambers could also be some type of gerontic kummerforms, because these chambers tend to be downsized and similar in shape, and this could indicate long life.
Abnormal apertures, which include three types: (a) aberrant shape (e.g., gaping aperture), usually associated with abnormal ultimate chambers (Fig. 5E1); (b) additional aperture (Fig. 5E2); and (c) multiple apertures (Fig. 5E3), usually associated with multiple ultimate chambers. According to Montgomery (1990), gaping apertures represent a strategy directly opposed to that of apertures covered by bullae, whose function is to protect them.
Distortion in test coiling, which includes three types: (a) excessively high spiral side or spiroconvex test (Fig. 5F1); (b) kinking (Fig. 5F2), that is, abnormal coiling due to a change in the direction of coiling, with two or more axes of rotation; and (c) twisting of entire test or extreme kinking (Fig. 5F3), that is, the umbilical side becomes the spiral side. Distortion in test coiling also seems to be a response to very stressed environments (Montogomery 1990; Polovodova and Schönfeld 2008).
Abnormal test, which includes four types: (a) lack of sculpture (Fig. 5G1); (b) poor development of the last whorl (Fig. 5G2); (c) overdevelopment of the last whorl (Fig. 5G3); and (d) compressed test (Fig. 5G4). Another test abnormality is a lack of ornamentation, but this type is not been analyzed here due to the difficulty of demonstrating the difference between abnormal alterations in the wall surface and the diagenetic processes of dissolution/recrystallization, which are usual in El Kef and Aïn Settara. As in the previous category, these abnormalities also seem to be a response to stressed environments (Polovodova and Schönfeld 2008), in some cases due to extremely stressful shifts in the environment (Montgomery 1990).
Attached twins or double tests, which include two types: (a) attached twins (Siamese) (Fig. 5H1), or even attached triplets (triamese) (Fig. 6.C); and (b) fused test (Fig. 5H2). If a second chamber beside the proloculus is followed by the development of an adjacent whorl, with two whorls with a similar number of chambers developing synchronously, attached twins are formed. Stouff et al. (1999) proposed that double tests in benthic foraminifera may result from: (i) an anomaly in the development of a single juvenile, building two or three second chambers or two third chambers, each one possibly developing in an individual whorl; (ii) the early fusion of two juveniles, which both develop after their fusion; (iii) the attachment of a juvenile to a parental test after schizogony, followed by the development of the juvenile specimen. According to Montgomery (1990), twinned specimens indicate reproductive difficulties in stressed environments.
General monstrosities (Fig. 5I): a conjunction of abnormal coiling due to several wrong directions of coiling, bulla-like kummerform chambers, double tests, and multiple ultimate chambers can generate monstrous abnormalities. Montgomery (1990) proposed that monstrosities are probably crushed and repaired specimens resulting from extremely stressful shifts in their environment or increased predation by organisms such as copepods.
According to Keller et al. (2011), Font et al. (2016), and Punekar et al. (2016), the main eruptive phase (phase 2) of the Deccan Traps may have been concentrated during the last ~50 or 100 Kyr of the Maastrichtian, triggering a short episode of global cooling—and ocean acidification—as a result of sulfate aerosol particles injected into the stratosphere and increased levels of mercury, an extremely toxic heavy metal. Opportunistic Guembelitria blooms have also been identified in the uppermost Maastrichtian, mainly in the shallow-marine environments of Israel, Egypt, Texas, and India, which suggests that the environmental deterioration and extinction began with the Deccan eruptions, several tens of thousands of years before the K/Pg boundary (Punekar et al. 2014; Keller et al. 2016). However, only minor Guembelitria blooms are present in the deep-marine environments of the Maastrichtian (Pardo and Keller 2008; Punekar et al. 2014). As proposed for warming episodes in the early Danian, Guembelitria acmes in shallow neritic environments could have also been under an orbital control related with small variations in sea level, temperature, acidity, and nutrients due to Milankovitch cycles (Quillévéré et al. 2008; Coccioni et al. 2010).
To test the hypothesis that the main eruptive phase (phase 2) of the Deccan Traps may have been concentrated during the last ~50 or 100 Kyr of the Maastrichtian, we have for the first time appraised the rate of aberrant planktic foraminifera in the upper part of the P. hantkeninoides Subzone from El Kef and Aïn Settara, as a proxy for ecological stress episodes. Our results indicate that there was a low frequency of aberrants (generally <2.5%) across this interval (Tables 1, 2), similar to the levels recorded in recent deep-ocean sediments under "normal" environmental conditions and reflecting the natural background number of malformations among planktic foraminifers (Mancin and Darling 2015). Low extinction and speciation rates, as well as low volatility and taxonomic flux fluctuations (Figs. 2 and 8), corroborate the high evolutionary stability that prevailed during the latest Maastrichtian in El Kef.
The causes proposed to explain the abnormalities in planktic foraminiferal tests are still very vague, including biological factors (such as unusually high levels of intraspecific variability) or various chemical and physical stressors (see Mancin and Darling 2015). For example, Coccioni and Luciani (2006) speculated that blooms of aberrant G. irregularis across the K/Pg boundary are explained as the result of rapid and extreme fluctuations in climate and sea level, as well as intense volcanism and meteoritic impact events, which could have stressed surface waters. The higher values in the FAI identified here during the first 200 Kyr of the Danian (affecting not only G. irregularis but all the planktic foraminiferal groups), however, require a better understanding of how the long-term effects of the Chicxulub impact or the paleoenvironmental changes induced by the Deccan eruptions affected planktic foraminiferal assemblages during the early Danian.
Model calculations have suggested several short-term (hour- to decade-long) environmental perturbations caused by the Chicxulub impact (see reviews in Kring 2007; Schulte et al. 2010; Brugger et al. 2017; Artemieva et al. 2017). These include a global pulse of increased thermal radiation on the ground and wildfires caused by the atmospheric re-entry of the ejecta spherules, the production of acid rain, and an injection of dust and aerosol particles into the atmosphere, blocking the sunlight. Using TEX86 paleothermometry, a short-term cooling (or "impact winter" phase) during the first months to decades following the Chicxulub impact has been documented at the Brazos River section in Texas (Vellekoop et al. 2014). Short-term global perturbations were likely major lethal factors for planktic foraminifera in the K/Pg mass extinction event (lasting months or a few years), but are insufficient to account for the increase of aberrants identified in the first 200 Kyr of the Danian.
Increased teratological forms in recent foraminifera are usually related with highly polluted areas (e.g., Alve 1991; Yanko et al. 1998; Geslin et al. 2002; Martin and Nesbitt 2015). Under the effect of extreme poisoning by heavy metals, the ability of foraminifera to constrain the shape of their shells is limited, leading to aberrant morphologies (Caron et al. 1987). The action of toxic heavy metals must have been very intense immediately after the Chicxulub impact. According to Erickson and Dickson (1987), a hypothetical 10-km-diameter chondritic impactor such as that of Chicxulub contains a mass of heavy metals, such as cobalt, nickel, copper, and mercury, comparable to or larger than the world ocean burden. Several heavy metals have relatively inefficient removal mechanisms, such as copper and nickel with greater than 1000-yr steady-state oceanic residence times. In addition, the worldwide sediments contaminated with heavy metals from the Chicxulub impact site may well have been eroded, removed, and resuspended in oceans for several thousand years (Smit and Romein 1985; Smit et al. 1996). Premovic et al. (2008) suggested that humics enriched in heavy metals were transported mainly by fluvial means into the ocean and deposited in the dark-clay bed. Enhanced levels of toxic heavy metals (e.g., nickel, zinc, chromium, cobalt, or copper) have been identified in the dark-clay bed, that is, in the first 10 Kyr after the K/Pg boundary, at Caravaca (Smit and ten Kate 1982), Aïn Settara (Dupuis et al. 2001), and Stevns Klint, Denmark (Premovic et al. 2008).
Chicxulub impact–linked chemical pollution could therefore be a major cause of the first bloom of aberrant planktic foraminifers within the dark-clay bed. In addition, the large amount of CO2 gas devolatilized in the Chicxulub impact and the collapse of ocean productivity and the biological pump initiated intense global warming through the greenhouse effect after the post-impact winter phase (Kawaragi et al. 2009), persisting as another ecological stress factor for thousands of years. Isotopic data from El Kef indicate a sudden negative excursion in bulk-sediment δ13C and δ18O after the K/Pg boundary (Keller and Lindinger 1989), suggesting a warming episode and a decrease in biological productivity at the time of the dark-clay bed deposition and PFAS-1. According to the GTS12 and the biochronological scale of Arenillas et al. (2004), this negative δ13C excursion lasted for the first 20–25 Kyr of the Danian.
Another potential cause of the first peak of aberrant planktic foraminifers in PFAS-1 could be phytoplankton blooms concentrating toxins in the surface waters (Jiang et al. 2010; Schueth et al. 2015). Toxicity is a well-known product of modern plankton blooms (Castle and Rodgers 2009), and geographically heterogeneous spikes of phytoplankton groups are reported in the earliest Danian. For example, quantitative analyses with organic-walled marine dinoflagellate cyst assemblages in the lowermost Danian of El Kef show a relevant acme of the Andalusiella–Palaeocystodinium complex between 10 and 15 cm above the K/Pg boundary (Brinkhuis et al. 1998). This peak correlates approximately with the initial increase in aberrant tests of planktic foraminifera at El Kef, but not with the maximum values recorded between 37 and 97 cm above the K/Pg boundary (Fig. 3, Table 1). Although phytoplankton blooms may have favored the concentration of toxins in the surface-water layers, more studies are needed to establish the relationship between such blooms and the proliferations of aberrant planktic foraminiferal tests in the early Danian. In any case, spikes of Andalusiella–Palaeocystodinium complex and other groups (such as the calcareous dinoflagellate cyst Thoracosphaera spp. or the nannofossil species Braarudosphaera bigelowii) identified in the Tethyan realm are usually explained as blooms of opportunistic taxa related to long-term environmental effects of the Chicxulub impact (Lamolda et al. 2005; Vellekoop et al. 2015).
On the basis of several independent stratigraphic, geochronological, geochemical, and tectonic constraints, Richards et al. (2015) hypothesized that the main Deccan eruptive phase (phase 2, >70% of the lava flows) could have been triggered by the Chicxulub impact during a relatively brief time interval on the order of one to several hundred thousand years. If this hypothesis by Richards et al. (2015) is correct, the long-term disruptive effects of the Chicxulub impact could be combined in the early Danian with those of Deccan volcanism, including a chemical contamination of the ocean surface over a longer period of time. This hypothesis could explain why the values of the FAI at the El Kef and Aïn Settara sections remained high during at least the first 200 Kyr after the Chicxulub impact (including the interval PFAS-2).
As mentioned earlier, the second increase in aberrant forms coincides with the Chiloguembelitria bloom in the lower part of PFAS-3 (Figs. 3, 8). This episode spanned between approximately 70 and 200 Kyr after the K/Pg boundary, so it cannot be related to the long-term disruptive effects of the Chicxulub impact. On the contrary, it seems that it was caused by another independent, later period of intense ecological stress perhaps linked to the Deccan eruptions (phase 2 or 3). Quillévéré et al. (2008) recognized in the lower Danian (in the E. trivialis Subzone, or Subzone P1a) a warming episode called Dan-C2 (the first hyperthermal episode of the Paleogene), which lasted approximately 100 Kyr. Although Dan-C2 and similar episodes could be a result of orbital cycles, Coccioni et al. (2010) proposed a possible link between this warming episode and the Deccan volcanism. According to this scenario, the second increase of the FAI, the Chiloguembelitria bloom, and the Dan-C2 episode could therefore be related. The low values of the FAI after the Chiloguembelitria bloom (in the S. triloculinoides Subzone, or Subzone P1b) suggest a period of greater environmental stability. This interval is widely dominated by biserial Woodringina and Chiloguembelina, typical of the PFAS-3 episode. Nevertheless, Coccioni et al. (2010) suggested that the predominance of biserials in Gubbio, along with other micropaleontological and geochemical proxies, was indicative of stressed ecological conditions (climatic warming and low oxygenation and acidification of ocean waters) during the Dan-C2 episode. According to this scenario, the whole PFAS-3 episode could be a record of the late eruptions of Deccan phase 2 or the first eruptions of phase 3. Moreover, the Chiloguembelitria bloom in the lower part of PFAS-3 could be the result of a more intense volcanic pulse during Dan-C2, though not one recorded at Gubbio by Coccioni et al. (2010).
Weinkauf et al. (2014) suggested that the phenotypic history of planktic foraminiferal assemblages allows the detection of threshold levels of ecological stress episodes that are likely to lead to extinction. According to these authors, an increase in interspecific morphological variability and abnormal forms can be observed at terminal stress levels immediately before extinction, indicating disruptive selection. In contrast, in periods of environmental stability and nonterminal stress levels, a decrease in morphological variability and abnormal forms is recognized, indicating stabilizing selection.
If the hypothesis that the massive eruptions of Deccan phase 2 were concentrated in the last 50 or 100 Kyr of the Maastrichtian and started a gradual mass extinction in planktic foraminifera before the K/Pg boundary (Punekar et al. 2016) is correct, a terminal stress episode with abundant aberrant forms should have been recorded below the K/Pg extinction horizon at El Kef and Aïn Settara. However, there is no evidence for such a scenario and, as in many sections worldwide, most Maastrichtian species suddenly become extinct at the K/Pg boundary following a catastrophic extinction pattern compatible with the short-term effects of the Chicxulub impact (Smit 1982, 1990; Huber 1996; Arz et al. 2000; Arenillas et al. 2000a,b; Huber et al. 2002; Molina et al. 2005; Gallala 2014). Similarly, latest Maastrichtian climatic fluctuations and environmental perturbations linked to Deccan volcanism had a relatively weak impact on the diversity of the calcareous nannoplankton assemblages before the K/Pg boundary, as evidenced in Elles and other sections worldwide (Thibault et al. 2016).
The first bloom of aberrants and PFAS-1 in the earliest Danian occurred in an interval in which the speciation rate was very high, especially in the lower part of the Pv. longiapertura Subzone, which also shows high volatility and relevant fluctuations in the taxonomic flux (Figs. 2 and 8). Arenillas et al. (2016) suggested that the speciation rate may have been increased in response to the long-term meteoritic pollution of the oceans, which may have caused increased mutation rates for at least 10 to 20 Kyr after the K/Pg boundary and triggered the first evolutionary radiation of planktic foraminifera. Many mutations in planktic foraminifera are likely to have been lethal, causing mortality before the adult stage was reached. However, genetic mutations could have accelerated the evolution of planktic foraminifera in the early Danian, being amplified as a consequence of stressed and adverse environments (BouDagher-Fadel 2012). In addition, many other mutations would have been deleterious, producing malformations and teratological forms, as has been proposed for recent foraminifera (e.g., Mancin and Darling 2015). The high values of the FAI identified in the dark-clay bed and PFAS-1 at El Kef and Aïn Settara are consistent with this hypothesis. This interval occurred during the survival and recovery phases after the K/Pg boundary extinction according to the terminology of Kauffman and Erwin (1995), in which Guembelitria included the "disaster species" and the minute parvularugoglobigerinids the "progenitor species" (Molina 2015), although the latter had a benthic origin, as has recently been proposed by Arenillas and Arz (2017). The evolutionary history of the planktic foraminifera was restarted almost from scratch after the K/Pg boundary extinction, suggesting that all the latest Maastrichtian species went extinct at the K/Pg boundary, except for some species of Guembelitria (see also Smit 1982; Arenillas et al. 2016).
The second bloom of aberrants and the Chiloguembelitria acme appear to be better adjusted to a terminal stress episode, as proposed by Weinkauf et al. (2014). Nonterminal stress episodes could correspond to PFAS-2, dominated by parvularugoglobigerinids and characterized by an aberrant rate lower than in PFAS-1 and the Chiloguembelitria acme. It is not possible to speak of environmental stability in PFAS-2, because values of the FAI and volatility remain high. In fact, the speciation rate in the upper part of PFAS-2 is high (Fig. 8) as a consequence of the beginning of the second evolutionary radiation. Nevertheless, the maximum in species richness (S=species number) of the early Danian is reached during the beginning of the Chiloguembelitria acme (Fig. 8), which represents a terminal stress episode. This is because the species that emerged during the first and second evolutionary radiations overlapped in time (Fig. 1). The parvularugoglobigerinids, which appeared in the first radiation, went extinct toward the end of the Chiloguembelitria acme, increasing the extinction rate (Fig. 8). Parvularugoglobigerinids were replaced definitively by the more ornamented, larger trochospiral species of the second evolutionary radiation. In this case, the Chiloguembelitria included the disaster species, and the species that appeared in the second radiation (those of Eoglobigerina, Parasubbotina, Globanomalina, and Praemurica, among others) were the progenitor species.
1. A high-resolution, quantitative biostratigraphic study across the K/Pg boundary from open-ocean Tunisian sections (El Kef and Aïn Settara) revealed a proliferation of aberrant planktic foraminifera during approximately the first 200 Kyr of the Danian. Various categories and types of abnormalities were identified, including abnormal tests, extra chambers, attached twin tests, and general monstrosities.
2. The proliferation of aberrants occurred in two main pulses. The first was more intense and occurred during the first 20 to 25 Kyr after the K/Pg boundary, spanning the dark-clay bed. It is characterized by abnormal forms of triserials (Guembelitria), but also of parvularugoglobigerinids (Parvularugoglobigerina and Palaeoglobigerina) from just the first evolutionary radiation of Danian planktic foraminifera. The second pulse is recorded between approximately 70 and 200 Kyr after the K/Pg boundary and is characterized mainly by abnormal forms of triserials (Chiloguembelitria) and biserials (Woodringina and Chiloguembelina).
3. These two pulses of aberrants correlate respectively with the Guembelitria acme in PFAS-1 and the dark-clay bed and with the Chiloguembelitria acme in the lower part of PFAS-3, both of which have been interpreted as ecological stress episodes. The FAI during the parvularugoglobigerinid acme in PFAS-2 is lower, but remains high enough to suggest that environmental conditions were also unstable during this interval, in which the second evolutionary radiation of Danian planktic foraminifera occurred.
4. According to the data set available here, the high values of the FAI in PFAS-1 seems to be more related to long-term environmental effects of the Chicxulub impact. By contrast, the second bloom of aberrants during the Chiloguembelitria acme was caused by an independent, later period of ecological stress perhaps linked to the Deccan eruptions.
5. The absence of an ecological stress episode rich in abnormal tests during the latest Maastrichtian in both the El Kef and Aïn Settara locations, as well as the high values of the FAI during the first 200 Kyr of the Danian, could be compatible with the hypothesis that the Chicxulub impact triggered the main phase of the Deccan Traps. This would render the Deccan volcanism an unlikely candidate as the cause of the K/Pg boundary mass extinction.
We thank I. Polovodova, C. M. Lowery, and two anonymous reviewers for their comments and critiques, which have greatly helped improve this paper. This study is a contribution to project CGL2015-64422-P (MINECO/FEDER-UE) and is also partially supported by the Departamento de Educación y Ciencia of the Aragonian Government, cofinanced by the European Social Fund (grant number DGA group E05). V.G. acknowledges support from the Spanish Ministerio de Economía, Industria y Competitividad (FPI grant BES-2016-077800). The authors would like to acknowledge the use of the Servicio General de Apoyo a la Investigación-SAI, Universidad de Zaragoza. The authors are grateful to Rupert Glasgow for improvement of the English text.
Biostratigraphic ranges of the early Danian species analyzed, based mainly on the El Kef and Aïn Settara sections, Tunisia; (1) planktic foraminiferal zonation and calibrated numerical ages of the biozonal boundaries proposed by Arenillas et al. (2004); (2) and (3) zonations of Berggren and Pearson (2005) and Li and Keller (1998), respectively; intervals with green shading indicate the first and second evolutionary radiations of the early Danian at El Kef (the shading in dark green indicates high speciation rates; see online version for color); dotted lines indicate uncertain ranges in the case of Guembelitria species (G. cretacea, G. blowi, and G. dammula) in the lower Danian, because these may actually correspond to reworked specimens and/or the ranges of morphologically similar species of Chiloguembelitria (Chg. danica, Chg. trilobata, and Chg. hofkeri, respectively). PFAS, planktic foraminiferal acme-stage.
Evolutionary metrics (extinction and speciation rates, volatility, and taxonomic flux) at El Kef according to the model of Dean and McKinney (2001); solid line, hypothesis of pattern A; dotted line, hypothesis of pattern B; green shading, episodes of evolutionary radiation, with shading in dark green to indicate high speciation rates (see online version for color). *Mh. holmdelensis Subzone (= Zone P0); **Pv. longiapertura Subzone.
Quantitative stratigraphic distribution of planktic foraminiferal groups and aberrant forms across the K/Pg boundary in the El Kef and Aïn Settara sections. The triserial group includes Guembelitria and Chiloguembelitria; the parvularugoglobigerinids include Pseudocaucasina, Palaeoglobigerina, and Parvularugoglobigerina; the biserial group includes Woodringina and Chiloguembelina; and other Danian genera include Trochoguembelitria, Eoglobigerina, Parasubbotina, Globanomalina, Praemurica, Subbotina, and Globoconusa. Curves with black shading represent the recalculated percentages assuming that, except for Guembelitria, the Maastrichtian specimens found in Danian horizons are reworked (pattern B hypothesis). Intervals with orange shading (see online version for color) represent terminal stress levels according to the model of Weinkauf et al. (2014). FAI, Foraminiferal Abnormality Index (% aberrant planktic foraminifera). *Mh. holmdelensis Subzone (= Zone P0); **Pv. longiapertura Subzone.
Schematic diagram of the main types of aberrant forms in the following categories: A, protuberances near the proloculus; B, chamber abnormalities; C, abnormalities of last chamber, including kummerforms; and D, multiple ultimate chambers, including double or twinned ultimate chambers (see explanation in text). Correlative normal forms are represented in miniature along with the abnormal forms.
Schematic diagram of the main types of aberrant forms in the following categories (continuing from Fig. 4): E, abnormal apertures, including multiple apertures; F, distortion in test coiling, including kinking; G, morphologically abnormal tests; H, double tests, including attached twins or fused tests; and I, general monstrosities (see explanation in text). Correlative normal forms are represented in miniature along with the abnormal forms.
Examples of extreme aberrant forms of early Danian planktic foraminifera. Scale bar, 100 microns. A and B, Guembelitria spp., multiple ultimate chambers (racemiguembeliform multiserial test). C, Guembelitria sp. (probably G. cretacea), attached triplets (triamese). D, Guembelitria sp. or Woodringina sp., general monstrosity (probably attached twins with abnormal, kummerform, and protuberant chambers). E, W. hornerstownensis, double or twinned ultimate chambers. F, Guembelitria sp. or Woodringina sp., general monstrosity (probably attached twins with abnormal chambers). G, Parvularugoglobigerina sp. or Palaeoglobigerina sp., general monstrosity. H, W. hornerstownensis, last chamber in anomalous position, with test going from biserial to uniserial. I,Pv. longiapertura, additional chambers and apertures. J, Palaeoglobigerina sp. (probably Pg. luterbacheri), attached twins (Siamese). K, Pv. sabina, bulla-like ultimate chamber. L, Pv. eugubina, twisting of entire test (extreme kinking) and overdeveloped last chambers. M, Parvularugoglobigerina sp. (probably Pv. longiapertura), two specimens with fused tests. N, Palaeoglobigerina sp., general monstrosity. O,Parvularugoglobigerina sp.; additional chambers and apertures. All specimens come from El Kef, except for some from Aïn Settara (E, F).
Examples of aberrant planktic foraminifera ordered by time intervals and environmental and evolutionary episodes. Scale bar, 100 microns. 1. Latest Maastrichtian: A, Heterohelix globulosa, kinking with change in the coiling direction. B, Pseudoguembelina kempensis, with multiple ultimate chambers. 2. PFAS-1 and transition between PFAS-1 and PFAS-2: C, Guembelitria sp. (probably G. cretacea), protuberant chambers. D and E, Guembelitria sp. (probably G. cretacea), welded chambers. F, Guembelitria sp. (probably G. cretacea), tetraserial form. G, Guembelitria sp. (probably G. cretacea), tetraserial form with multiple apertures. H, W. claytonensis, abnormal test with overdeveloped or inflated chambers. I, Guembelitria sp., multiple ultimate chambers (racemiguembeliform multiserial test). J, Chiloguembelitria sp. (probably Chg. trilobata), attached twins (Siamese). 3. PFAS-2: K, Pg. luterbacheri, double twinned chambers. L, Pv. sabina, bulla-like ultimate chamber. M, Parvularugoglobigerina sp., bulla-like ultimate chamber. N, Pv. eugubina, protuberant aberrant chamber. O, Pv. longiapertura, abnormally spiroconvex test. 4. Lower part of PFAS-3 (Chiloguembelitria acme): P, W. claytonensis?, general monstrosities, probably attached twins (Siamese) with abnormal chambers. Q, W. hornerstownensis, kinking with change in the coiling direction. R, W. claytonensis, kinking with change in the coiling direction and last chambers apparently protuberant. S, W. claytonensis, reduced last chamber (kummerform). T, Ch. taurica, last chamber in anomalous position, with test going from biserial to triserial. U, W. claytonensis, last chamber in anomalous position, with test going from biserial to uniserial. Most of the specimens come from El Kef, and the rest are from Aïn Settara (F, P, Q), Elles (G, K), Agost (O), and Caravaca (T).
Shifts in specific richness (species number), speciation rate and volatility (according to the model of Dean and McKinney, 2001), relative abundance (%) of triserial specimens, and FAI (rate of aberrants in %) across the K/Pg boundary at El Kef; solid line and gray shading: hypothesis of pattern A; dotted line and black shading: hypothesis of pattern B; orange shading: terminal stress levels according to the model of Weinkauf et al. (2014), A corresponding to PFAS-1 and B to the Chiloguembelitria acme; green shading, evolutionary radiations, with shading in dark green to indicate high speciation rates (see online version for color). FAI, Foraminiferal Abnormality Index (% aberrant planktic foraminifera). *Mh. holmdelensis Subzone (= Zone P0); **Pv. longiapertura Subzone.
Relative abundance (%) of planktic foraminiferal groups considered here and rates of aberrants at the El Kef section. Values for the hypotheses of both pattern A and pattern B are included. A. m., Abathomphalus mayaroensis Zone; P. h., Plummerita hantkeninoides Subzone; H. p., Heterohelix predominance; P. e., Parvularugoglobigerina eugubina Zone; P. s., Palaeoglobigerina sabina Subzone. Samples are presented in centimeters below (−) and above (+) the K/Pg boundary. x, relative abundance <0.3%.
Relative abundance (%) of planktic foraminiferal groups considered here and rates of aberrants at the Aïn Settara section. Values for the hypotheses of both pattern A and pattern B are included. A. m., Abathomphalus mayaroensis Zone; P. h., Plummerita hantkeninoides Subzone; H. p., Heterohelix predominance. Samples are stated in centimeters below (−) and above (+) the K/Pg boundary.
N36°10'60" - N36°10'60", E08°43'00" - E08°43'00"
. Guembelitria irregularis bloom at the K-T boundary: morphological abnormalities induced by impact-related extreme environmental stress?. Pp.
. Unravelling the Cretaceous–Paleogene (KT) turnover: evidence from flora, fauna and geology. Pp.
Twin and bilobated chambered Cretaceous planktonic foraminifera: abnormal forms induced by high paleoenvironmental stress?


text:
in: Episode, Watch Dogs
Watch_Dogs: Too Much Sandbox, Too Little Game
This week, Zero Punctuation reviews WATCH_DOGS.
The hype train for Watch_Dogs had all the grace and subtlety of a 19th-century steam locomotive dangerously overloaded with jizz cannons and jizz cannon maintenance equipment. Which, as we've often learned, can be the warning sign that the publishers don't have a lot of faith in the game being able to stand upon its own merits. Well, it certainly can't stand upon its understanding of how hacking works, I can tell you that straight away! Basically, if your hackers are mostly hip young DJs and tattoo artists who all cribbed their sense of style from the halfway point between My Little Pony and Pinhead from Hellraiser, and have been so obviously workshopped to oblivion that they might as well be snapping their fingers and referring to authority figures as "daddy-o", then you are already showing your ignorance, 'cause most hackers are fat, greasy shit-minglers with terrible beards, posting Google Street View images of the houses of people who think we should have to pay money to watch TV shows. What will certainly not help is having your hackers put on very serious faces and wave their handheld devices about the way Marvo the Master Wizard works his magic wand!
Fortunately, the protagonist of Watch Underscore Dogs is not one of the heavily-workshopped Johnny Lee Miller rejects, but Aiden Pearce, a character who appears to have had all personality sandblasted off, 'til he's a blank cipher who doesn't even know how to button a trench coat properly. He was a hacker who did any work for hire and stole money from bank accounts, but then accidentally targeted someone powerful who killed his six-year-old niece, which gave him a little Spiderman moment and he declared that from this day forth he would use his powers to… continue working for hire and stealing money from bank accounts, but also fight crime! In-between. If he can be arsed. Not stealing-money crime, or property-damage crime, or murdering-policemen crime; just, you know, all the bad crimes, the ones committed by people other than himself. Oh, but no one can understand Aiden's pain! Other than, you know, the kid's mother, his sister, who seems to be infinitely better-adjusted about the whole thing. But then, she also hasn't figured out that Aiden is the mystery vigilante even after the news media starts broadcasting his name, so she's probably a few dead kids shy of an origin story.
Watch_Dogs isn't an easy game to summarize. The elevator pitch must have been delivered during a massive power outage. I suppose you could refer to it as "Assassin's Creed in the future". Might as well, it's got about the same amount of stabbing as Assassins's Creed does these days. Main difference is that instead of using rooftop vantage points to plan ahead, you use security cameras, and I'd say that's where the game comes onto its own: when you learn to think outside of the little bland cardboard cut-out of a man we have been insolently asked to identify with and turn the environment to your advantage, creating distractions and blowing up people who come to look at them, which never stops being funny.
"Gosh, I'm curious about that dog barking sound! Gosh, I'm curious as to where my legs landed!"
It falls apart pretty quick when the enemies spot you, because Aiden Pearce in a firefight has the durability of a Pringle between a professional wrestler's buttocks. But at least that provides incentive to use all these mechanics. In this age of namby-pamby, "play-it-your-way", psychotic mass-market inclusiveness, more games should have the apricots to draw the line and say, "You'll do it the way we like, or you'll do it with more bits of metal in you than your love interest's face".
But at other times, Watch_Dogs has the old Assassin's Creed problem with getting easy shortcuts confused with gameplay innovation. For example, if Assassin's Creed II wanted someone dead, you had to creep unnoticed into close enough range to stab him up the brisket. But by AC Brotherhood, you're free to crossbow them from two rooftops away when you're not just handing it off to the intern. In Watch_Dogs, you can hack traffic lights and barriers to discourage pursuers, but how that applies is that a quick-time event flashes up as you drive along the road, you press it, and hey presto, pursuer fucks off. Thank goodness, I was coming dangerously close to waking up!
And Sass-o Creed-o at its worst always seems to be just assembling a big disconnected pile of stuff to do as opposed to a cohesive whole, which in theory is something for everyone, but in practice is like hiding someone's birthday present in a room filled floor-to-ceiling with ping pong balls.
All Watch_Dogs' fun side activities are outnumbered by shit ones. The ones I found most specifically vexing were the random crimes. How they work is that a "crimer" and a "crimee" get together, and the moment crime starts, you leap in and brain the offending party with a stick, ideally before the victim gets hurt. But something like five times in a row I failed the mission because I jumped in nanoseconds before the event had been officially declared a crime. So I'd see one of the dudes raise a gun or a big knife and then I'd leap out yelling, "What's all this then!?", whereupon the criminal would go, "Well, that completely ruined the mood, you asshole!" and then skip off, hand in hand with the erstwhile victim, leaving me with the game saying, "I hope you're proud of yourself."
But the main thing that kills the sandbox activities is that there's bugger-all they can reward you with. Money only buys weapons and craft items that are all lying around for free anyway, and the character upgrades are as enticing as Chuck E. Cheese prizes:
"Here's one that lets you steal more money!"
Not gonna dignify that with a reply.
"How about the ability to resist tire blowouts?"
I only had a tire blowout once in the entire sodding game; I just nicked another car. Give me something I can use, like a thing that makes enemies drop dead when Aiden Pearce says something boring!
The ability to disable pursuing helicopters is useful, but it would be most useful from a getaway car, and the camera won't look straight upwards while you're in a car, so you can't get line-of-sight. I had to stop the car, sirens blaring all around, stand there in the street like a knob as the police snipers took aim, and point gormlessly at the helicopter like a man with a wonky garage door remote.
Watch_Dogs does not live up to the hype, but that's hardly fair, because it would need to have made me spontaneously grow a third bollock to do that. A predictable story with no likable characters – Aiden and his sister both look at the grave of the child that is his whole motivation the way they'd look at a middling-difficulty sudoku puzzle – and the gameplay is a lot of faff and chaff packed around one or two core ideas with potential.
I really liked the two or three missions where you stay on the cameras and guide an accomplice from cover to cover, because at that point, you're basically playing as the tutorial voice in somebody else's video game. They make a whole game of that, I think it would do alright, because any measure that will minimize the amount of time Aiden Pearce's burbling little face has to appear on-screen is worth about twelve Game of the Year awards right there!
Keep an eye on this motherfucker: Ben "Yahtzee" Croshaw
Here's a simple hack for you – stand in the middle of a street and wave your smartphone around and hey presto! You've just been mugged
This was Watch Dogs Review Special Edition #5,789

redpajama_set_name: RedPajamaCommonCrawl


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Busted! 3 myths about timber construction
Home Infrastructure Construction & Civils Busted! 3 myths about timber construction
InfrastructureConstruction & CivilsEnvironmental – Green IndustriesAgricultureForestryManufacturing & ProcessingPulp & Paper
By Roanna
WHILE timber construction has a relatively small footprint in South Africa, the building material is enjoying increasing popularity and interest among the general public and trade alike. Even so, misconceptions about timber as a construction material are still commonplace, limiting potential users from enjoying the manifold benefits of this unique, renewable building material.
That's according to Dr Brand Wessels, Chairperson of the Department of Forest and Wood Science at the University of Stellenbosch, who said the three most common myths that circulate among the general public and even the professional trade about timber as a building material are that using trees to manufacture products is not environmentally responsible; that wood structures are not as structurally safe and durable as steel or brick and mortar structures; and that wood structures are an obvious fire hazard.
Plantations, not natural forests
On the notion that using trees to manufacture products is environmentally irresponsible, Wessels said there was a distinct difference between harvesting timber from sustainable and well-managed plantations and the deforestation and degradation of natural forests that should be protected.
"In South Africa, we use timber grown in responsibly managed plantations, which are like working factories with the sole purpose of growing timber in a controlled environment for the market. Managed by reputable bodies like the Forest Stewardship Council (FSC), these plantations are operated in line with the highest standards for ensuring sustainability."
He cited recent studies, including one carried out in South Africa, which show that tree planting and forest restoration are the most cost-effective strategies with the greatest potential of combatting global climate change.
Contrary to the misconception that timber structures are not structurally safe and durable, timber has a higher strength-to-weight ratio than either steel or brick and mortar, said Wessels.
"This misconception may be linked to perceptions around low-cost, poorly built informal housing of wood. On the contrary, in some applications, such as for housing in earthquake-prone areas, wood is preferred above other materials. There are structures that are 1200 years old in Japan (an earthquake-prone country), which attest to the material's durability and strength.
"As with any other material, a well-designed and built wood structure will last a lifetime; conversely, a poorly designed and built structure – of any material – will not endure."
According to Amanda Obbes, General Manager of the Institute for Timber Construction South Africa (ITC-SA), timber frame construction is a standard construction methodology under the National Building Regulations (NBR), which provide the necessary building codes for the manufacture and construction of safe, legal and durable structures that are built to standard.
Timber under fire conditions
According to the ITC-SA, structural timber for roofing is both commonplace and performs well under fire conditions.
As with every aspect of building, timber roof trusses must be manufactured and erected in line with the National Building Regulations and SANS 10400, which provide for fire safety. Building regulations, set in place by bodies such as the South African Bureau of Standards (SABS) after extensive research and consultation with industry experts, consider all aspects of a given building material's composition and properties to ensure that it meets the same safety and performance standard as any other building material in the same application.
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The attic is the main part of the house and ensuring the proper ventilation and air flow of the house should be your first priority. People often ignore to maintain the attic as it is the most unseen part of the house, however, a good attic can give the home a good air flow and keeps the house warm regardless any temperature. So tilt your head up and look at the necessary requirements for your attic at home.
A ventilation is necessary to ensure that the house has required air flow through vents and exhausts. It keeps the house cool during summer and warm in winters. The house should have facilities that allow the air from the house to go from the exhaust and fresh air come from the inlet and this can be accommodated only through proper ventilation.
Hearing Noises in Your Attic at Night? You May Have Wild Animals in Your Attic! This is our childhood nightmare and the reason behind this is the improper insulation. Make sure that the attic is insulated well and there are no empty spots in them, the house can damage the attic turning the heat radiation high. A good insulation is mandatory for the house with the continuous inspection of the same. Any insulation that looks worn out, noisy or has water leakages should be changed immediately.
You may not check your roof often unless it rains or snows heavily and you happen to notice your roof has a leak in it This is the most ignored part of most of the houses, the unattended roofs. The moisture is the roof gets accumulated due to which the roofs experience cracks and finally results in leakage that also damages your inner flooring. It is advisable to check the leaks often with the help of professionals or someone who know the trick of checking the roof leaks.
As you clean the house to avoid dust, make sure to clean your attic well The dust and webs are accumulated are most likely to be accumulated in the attic space when compared to the other part of the houses. Cleaning the attic can be a hard task, however, you can take professional help or can consider to do it alone with all the necessary things available in the market for cleaning.
The tiny gaps and the holes in the attic can cause major issues for your home, these are the home for bugs and pests. Accumulating the pests in the attic is really not hygienic because it stops the air from flowing freely and blocks even the vents. Thus, always check for such holes and seal them well and clean up all the dust and dirt that are making its place in the attic.
These simple tricks can keep the attic safe and hygienic and in turn help you and your family with proper ventilation and healthy flow of air.
This entry was posted in Home & Garden and tagged attic, maintain on January 27, 2017 by writerbc.


Brad Plumer has a useful piece today about Sen. Tom Coburn's "Wastebook 2010," which allegedly exposes massive amounts of waste, fraud and abuse in the federal budget. You should read it, but I want to add a separate comment.
I'd venture to guess that barely any organization in human history has managed to reduce WFA below about 2%. If you earn $50,000 a year, that means waste of $1,000. Even careful households probably piss away that much each year. If you run a million-dollar small business, it means waste of $20,000 a year. Again: even a very miserly small business probably loses that much. It's just impossible to keep track of every expenditure, monitor every employee every minute of the day, or make sure you get the best price on every possible purchase.
Probably no one would argue too much about this because these numbers are human size. An average family blows a hundred bucks a month on dumb stuff? Sure. A business with half a dozen employees makes $20,000 worth of mistakes each year? Sure. But what about a federal government that spends upwards of $3 trillion per year? The same rate of WFA amounts to $50 billion or more. Or, using the usual budget window, $500 billion over ten years. That seems like an outlandish amount, but it's actually the same 2% as everyone else.
None of this is to say that we shouldn't fight this stuff. Families should, small businesses should, and the government should. Hell, Coburn's book might be a public service. But even if we do a rip-roaring job of fighting WFA and run the cleanest government in human history, any decent investigator will still probably be able to find at least 2% waste in the system. It seems like a huge amount, but it's largely a mirage based on people getting fooled by numbers too big for human comprehension. This happens a lot in modern society.
However, a definition that includes any kind of abduction, even those lasting only a few minutes or a few hours, brings the tally up to 58,000 per year — and obviously parents are concerned about these kinds of abductions too. Some of them are what you'd think of as child snatchings and some aren't, but in any case the number is far higher than 115. Using the broader definition, the odds of having your child snatched is (depending on how broadly you cast your net) one in a thousand or less, which is quite low but still nowhere near the odds of being struck by lightning.


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Android News / All News / Samsung Galaxy S4 Google Play Edition Finally No Longer Available
Samsung Galaxy S4 Google Play Edition Finally No Longer Available
The 2013 Samsung Galaxy S4 gave the world the first Google Play Edition device and the one that might be given the credit for helping HTC's decision to release their 2013 flagship device, the HTC One (M7), as a Google Play Edition. It's been showing as out of stock for some time now on the Google Play Devices webpage and today the status has been updated to show that it is no longer available. This is perhaps understandable given that the handset is approaching two years old, leaving just four devices available in the Google Play Devices: the Nexus 5, Nexus 6, Nexus 9 and HTC One (M8). The S4 is certainly capable of running the current version of Android. It's based around a 5.0-inch, Samsung Super AMOLED screen of 1080p resolution. The handset uses a 1.9 GHz quad core Qualcomm Snapdragon 600 processor backed up by 2 GB of RAM and with 16 GB of internal storage, plus a MicroSD card slot. The S4 uses a 13 MP rear camera and a 2 MP front facing camera. It's kept alive by a 2,600 mAh replaceable, rechargeable battery; these specifications are no longer cutting edge but with the S4 running stock Android, it's still as smooth and fluid as Android Lollipop is (at least for the first forty hours, anyway).
Google Play Edition devices are an interesting way to access Android. They're almost a Nexus device, but not quite. Their advantage is that you can take software that's very close to stock (Google Nexus) Android but with other features: the S4 Google Play Edition came with a better camera, screen, battery and of course a MicroSD card slot compared with the LG Nexus 4. Unfortunately, the Google Play Edition Galaxy S4 was also considerably more expensive than the Nexus 4… And now the S4 Google Play Edition joins the retired Google Play Edition versions of the Sony Xperia Z Ultra, HTC One M7 and Motorola Moto G, what do we have to look forward to from the manufacturers? Are the big names going to release Google Play Editions of their 2015 devices? Or were the sales too disappointing?
Some manufacturers have already aligned their handset software with stock Android, such as Motorola and Sharp, such that there's arguably no point in releasing a Google Play Edition version. Was there so much difference between the original Moto G and the Google Play Edition? For other manufacturers, such as HTC, the Google Play Edition missed out on many of the "special sauce" features that made gave the original device a certain charm. Of course, for those of us who insist on nothing but stock answer, we already have our answer here! Over to our readers; will you miss the Google Play Edition version of the Galaxy S4? Did it add more to the Google universe than it detracted? Let us know in the comments below.


A move from the New York Design Center to the fancy mall in the old Tunnel nightclub. The schoolgirl from Wrexham in Wales, was approached by somebody using Snapchat under the name New Faces Models and asked to send 'something that shows off her body and figure.' deltasone After the hashtag ExposeChristianSchools went viral, we invited readers to tell us about how their Christian school educations shaped their lives.