Beyond India, multi-proxy studies also place the main Deccan phase in the uppermost Maastrichtian C29r below the KTB, as indicated by a rapid shift in 187Os/188Os ratios in deep-sea sections from the Atlantic, Pacific and Indian Oceans, coincident with rapid climate warming, coeval increase in weathering, a significant decrease in bulk carbonate indicative of acidification due to volcanic SO2, and major biotic stress conditions expressed in species dwarfing and decreased abundance in calcareous microfossils (planktic foraminifera and nannofossils, Fig. 2). These observations indicate that Deccan volcanism played a key role in increasing atmospheric CO2 and SO2 levels that resulted in global warming and acidified oceans, respectively, increasing biotic stress that predisposed faunas to eventual extinction at the KTB.
Figure 1. Over 150 KTB sections have been analyzed worldwide over the past 25 years by Keller and her students and collaborators. This research has resulted in a global database that permits the evaluation of the environmental and biological effects of both the Chicxulub impact and Deccan volcanism.
Planktic Foraminifera as Environmental Proxies
Planktic Foraminifera are excellent proxies for high-stress conditions associated with greenhouse warming, mesotrophic to eutrophic waters, marginal settings, and volcanically active regions during the Late Maastrichtian and early Danian. Sedimentary sequences analyzed from Israel, Egypt, Tunisia, Texas, Argentina, India and Indian Ocean (Fig. 1) reveal that the biotic response varies from optimum to catastrophic with the degree of biotic stress related to variations in oxygen, salinity, temperature, pH and nutrients (Pardo and Keller, 2008; Keller and Abramovich, 2009).
Figure 2. Size and shapes of tests of Maastrichtian planktic foraminifera species showing a continuum from small r-strategists to large complex k-strategists. R-strategy and opportunistic life strategy of Guembelitria are inferred by their minute test size, simple chamber arrangement and isotopically light d13C values. K-strategy species are inferred from large and complex test morphology, small populations and heavier d13C values. From Keller and Abramovich, 2009.
Planktic foraminifera vary in test sizes from very small to very large, from unornamented to highly decorated tests, from simple morphologies to the very complex (Fig. 2). These characteristics reflect the degree of environmental stress that species can tolerate and the particular ecological niches they tend to inhabit.
Â· K-strategists are large, morphologically complex, highly ornamented and very diverse species group. They utilize particular food sources and specialize in particular ecological niches; they have longer life spans and tend to produce only small numbers of offspring.
Â· R-strategists are the small to medium sized species with unornamented tests and simple morphologies. They have low species diversity, utilize a variety of food sources, live under variable environmental conditions, live short life spans and have a large number of offspring.
R-strategists thus optimize chances for survival, whereas k-strategists optimize the good life while it lasts.
From Optimum to High-Stress Conditions
Early stages of biotic stress result in diversity reduction and the elimination of large specialized species, followed by size reduction (dwarfism) of survivors and dominance of low O2 tolerant species (heterohelicids). At the extreme end of the biotic response are volcanically influenced environments, which cause the same detrimental effects as observed in the aftermath of the KT mass extinction, including the disappearance of most species and blooms of the disaster opportunist Guembelitria (Fig. 3).
Figure 3. The effects of increasing environmental stress upon planktic foraminiferal assemblages from optimum to catastrophe conditions shows the successive elimination of large, specialized k-strategy species, the survival of small r-strategy species, the overall dwarfing of these species and their great abundance. From Keller and Abramovich, 2009.
Late Maastrichtian environments span a continuum from optimum conditions to the catastrophic (mass extinctions) with a predictable set of biotic responses relative to the degree of stress induced by oxygen, salinity, temperature and nutrient variations as a result of climate and sea level changes and volcanism.
Â· Early stages of biotic stress result in diversity reduction and the elimination of large specialized species (k-strategists) leading to morphologic size reduction via selective extinctions and disappearances and intraspecies dwarfing of survivors.
Â· Later stages of biotic stress result in the complete disappearance of k-strategists, intraspecies dwarfing of r-strategists and dominance by low oxygen tolerant small heterohelicids.
Â· At the extreme end of the biotic response are volcanically influenced environments, which cause the same detrimental biotic effects as observed in the aftermath of the K-T mass extinction, including the disappearance of most species and blooms of the disaster opportunist Guembelitria.
Specialists under Stress (K-strategists)
Dwarfing (also called the Lilliput effect) of large specialized species has been observed in association with the latest Maastrichtian climate warming, which has been attributed to Deccan volcanism (Kucera and Malmgren, 1998; Olsson et al., 2001; Abramovich and Keller, 2003; Keller and Pardo, 2004).
At Site 525A on Walvis Ridge, South Atlantic the latest Maastrichtian warm event is documented in a high resolution stable isotope analysis by Li and Keller (l998a, b, c) and tied to high-stress conditions in planktic foraminiferal assemblages by Abramovich and Keller (2003). The size reduction in these assemblages is over 50%. High-stress conditions also resulted in decreased abundance of Heterohelix species, and increased abundance of dwarfed specimens.
Fig. 4. Species dwarfing (50% reduced size) during the latest Maastrichtian C29r warm event at DSDP Site 525 on Walvis Ridge, South Atlantic (From Abramovich and Keller, 2003; stable isotopes from Li and Keller, 1998b).
K-strategists meet Disaster
When a major environmental perturbation dramatically alters the ecosystem, the result may be mass mortality. The KTB mass extinction decimated planktic foraminiferal assemblages, eliminating all tropical and subtropical k-strategy taxa, which accounted for about 2/3 of the species assemblage. The k-strategistsâ€™ tenuous hold on survival even before KTB time is evident by the fact that their combined relative abundance was already less than 5% of the total foraminiferal population during the latest Maastrichtian zone CF1, which spans the last 300,000 years of the Maastrichtian.
Clearly, specialized species suffered mass mortality well before their extinction at the KTB. In the past, this abundance decline in large specialized species has been attributed to climate and sea-level changes, for lack of a better explanation. But this explanation was never very satisfactory because climate and sea-level changes occur continuously in Earth history without causing mass mortality and mass extinctions. It now appears likely that Deccan volcanism was the major cause for the early demise of these species as well as their later extinction at the KTB (see Deccan volcanism website).
Opportunists Inherit the World
Only r-strategists survived in the immediate aftermath of the mass extinction (e.g., heterohelicids, hedbergellids, guembelitrids, Fig. 8). Among this group, the subsurface dwellers Hedbergella and Heterohelix (H. globulosa, H. navarroensis) survived well into the Danian but with very reduced populations (Keller and Abramovich, 2009).
Only the disaster opportunist Guembelitria species thrived and dominated the assemblages (80-100%) after the mass extinction, then decreased as competition grew with the newly evolved Danian species.
Guembelitria, the smallest Cretaceous planktic foraminiferal species, are also the oldest survivors in foraminiferal populations and their morphotype is still around today. Stable isotope ranking indicates that they thrived in nutrient-rich surface waters where few or no other species survived (Pardo and Keller, 2008).
Opportunists and Volcanism
Biotic effects attributable to volcanism are still poorly understood. Studies of volcanic or pollution effects in Recent sediments, reveal decreased diversity, dwarfing and growth abnormalities in foraminifera (Yanko et al., 1994; Hess and Kuhnt, 1996). Similar biotic effects have also been observed in foraminifera associated with Deccan volcanism (e.g., Meghalaya). Perhaps the clearest example of the biotic effects of volcanism is found in the late Maastrichtian of DSDP Site 216 on Ninetyeast Ridge (Keller, 2003, 2005). Another example is the NeuquÃ©n Basin of Argentina (Keller et al., 2007).
Ninetyeast Ridge DSDP Site 216, Indian Ocean:
This locality tracks the passage of the oceanic plate over a superheated mantle plume during the late Maastrichtian (zone CF3). During this passage, lithospheric uplift led to the formation of islands built to sea level, and volcanic activity continued for more than 1 million years leading to catastrophic environmental conditions for marine life (Keller, 2003, 2005).
The biotic effects were severe and immediate, eliminating all species in the vicinity of the volcanic eruptions. As Site 216 moved past the immediate reach of mantle plume volcanism, sediments changed from basalt to phosphatic volcanic clay and black vesicular glass, and environmental conditions improved sufficiently for the small disaster opportunists Guembelitria to return and dominate (85-100%). Only a minor component of other r-strategists returned at this time with all species dwarfed (<100 Âµm, e.g., Heterohelix, Hedbergella and Globigerinelloides), species richness only between 4 and 10 species and d13C values well below normal marine productivity (Fig. 5).
With varying intensity of volcanic influx over time, the disaster opportunists Guembelitria and low oxygen tolerant Heterohelix species alternately dominated, whereas the abundance of surface dwellers remained low. Only after significantly reduced volcanic influx, a change to glauconite-rich chalk and an abrupt increase in d13C values do Guembelitria disappear, species richness increase to 15 and species size increase, returning to near normal for r-strategists and signaling improved environmental conditions (Fig. 5).
Figure 5. Foraminiferal response to Ninetyeast Ridge volcanism during the late Maastrichtian. From Keller, 2003.
Andean Volcanism â€“ Effects in Argentina
During the late Maastrichtian (zones CF4-CF2) to early Danian, the NeuquÃ©n Basin of Argentina was adjacent to an active volcanic arc. Marine conditions were maintained through an open seaway to the South Atlantic. At the Bajada de JagÃ¼el section sediment deposition occurred in a shallow inner-neritic to middle-neritic environment (50-100 m) with fluctuating sea level and dysaerobic conditions (Keller et al., 2007).
Volcanic influx into this environment occurred as ash fallout during eruptions and from continental runoff via erosion. Within this environment, planktic foraminifera mimic the post-KTB high-stress environment with alternating blooms of the disaster opportunist Guembelitria (G. cretacea and G. dammula) and low oxygen tolerant but dwarfed Heterohelix species (e.g.. H. globulosa, H. dentata, Zeauvigerina waiparaensis). Other small r-strategy species are rare (e.g., Hedbergella, Globigerinelloides aspera) (Fig. 6).
These high-stress assemblages suggest nutrient-rich surface waters and an oxygen depleted water column as a direct result of weathering and high continental influx, as indicated by clay and bulk rock minerals (Keller et al., 2007). Species richness is very low ranging from 2 to 7, except for a brief incursion of dwarfed k-strategists (e.g., Rugoglobigerina rugosa, R. macrocephala, Globotruncana arca, G. aegyptiaca, Gansserina gansseri) during climatic warming and a rise in sea-level (Keller et al., 2003, 2005).
Figure 6. Foraminiferal response to volcanism in the NeuquÃ©n Basin of Argentina; alternating Guembelitria and Heterohelix blooms mark variations in intensity of environmental stress. From Keller et al., 2007.
Effects of Deccan Volcanism in the Tethys
Most studies have concentrated on Guembelitria blooms in the aftermath of the KTB mass extinction as evidence for the most severe environmental conditions (see review in Pardo and Keller, 2008). Less studied are the Guembelitria blooms of other high-stress periods, particularly during the late Maastrichtian. Indeed, it is those high-stress environments that provide insights to what may have happened at the end of the Cretaceous.
Unusual Guembelitria blooms were observed in the Qreya section of central Egypt during the late Maastrichtian. The high abundance of these disaster opportunists mimics blooms known globally in the aftermath of the KTB mass extinction (Keller, 2002). Similar Guembelitria blooms have been observed in Israel (Abramovich et al., 1998; Keller et al., 2004). Sediment deposition occurred in a middle-neritic environment in central Egypt and in a deeper outer-neritic environment in Israel.
Figure 7. Foraminiferal response to high-stress conditions in Egypt; alternating Guembelitria and Heterohelix blooms mark variations in intensity of environmental stress. Stress conditions may be related to Deccan volcanism. From Keller, 2002.
At the Qreiya section, the KTB is marked by a thin clay layer and Ir anomaly above a bioturbated marly shale with an erosional surface. Hiatuses also reduced early Danian zones Pla, Plb and Plc (Fig. 7). Guembelitria blooms are present in the early Danian zones Pla and Plc, similar to other Tethys sections (Keller, 2002).
What sets Qreiya apart from other KTB sections are the Guembelitria blooms (50-70%) in the upper Maastrichtian zones CF4-CF3 and CF1. At times of low Guembelitria abundances, the small Heterohelix navarroensis dominates. Species richness is also very low (25-30 species) compared with similar paleodepths at Elles (40-45 species).
These Guembelitria blooms indicate that the late Maastrichtian of the eastern Tethys experienced similar high stress conditions as the lower Danian in the aftermath of the mass extinction. d13C data indicate only a minor (0.7 â€°) negative excursion at the KT boundary, suggesting that primary productivity was already reduced during the upper Maastrichtian, as also indicated by the low species richness, Guembelitria blooms and small Heterohelix species. Low primary productivity is also indicated by the upper Maastrichtian reversal in the surface-to-deep d13C gradient, which is usually associated with the KTB productivity crash. It is possible that these Guembelitria blooms are due to high stress conditions related to the three phases of Deccan volcanism. Further work is needed to explore this possibility.
Tethys and the Effects of Deccan Volcanism
Deccan Phase-2 Volcanism:
In India outcrops and cores reveal Guembelitria cretacea blooms directly associated with the main Deccan phase-2 volcanism in chron 29r and correlative with zones CF1-CF2, which span the last 160ky and 120ky, respectively. These Guembelitria blooms are similar to those documented worldwide in previous studies done at a time when a connection to Deccan volcanism was highly speculative and no direct link to the KTB mass extinction had been established (Keller and Pardo, 2004; Pardo and Keller, 2008; Keller and Abramovich, 2009).
Figure 8. Correlation of Guembelitria bloom events in the late Maastrichtian of the eastern Tethys (Israel, Egypt) and Western Interior Seaway (Brazos, Texas) correlated with the climate record of South Atlantic DSDP Site 525A and Deccan volcanism phase-1, phase-2 and phase-3.
Today a link to global high-stress conditions (Guembelitria blooms) can be demonstrated for Deccan phase-2 leading up to the KTB mass extinction (Fig. 8) in India, the eastern Tethys (Israel, Egypt) and Texas (Keller and Benjamini, 1991, Abramovich et al., 1998; Keller et al., 2004, 2009). These high-stress conditions coincide with the global warm event in CF1-CF2 (see also Fig. 4) and directly correlate with the super-stress conditions documented in Meghalaya (see website on Deccan volcanism).
Deccan Phase-1 Volcanism:
Even the comparatively minor phase-1 of Deccan eruptions left its global mark. Analysis of ONGC wells from the Cauvery Basin reveal the first link to the onset of Deccan volcanism in zone CF4 (~67.5 m.y.) based on ash fall and blooms of the disaster opportunist Guembelitria cretacea. Faunal analysis of the same interval in the eastern Tethys (Israel, Egypt, Tunisia) and Texas reveal correlative Guembelitria blooms that indicate strong adverse global effects associated with phase-1 Deccan volcanism (Fig. 8).
Deccan Phase-3 â€“ Volcanism
Deccan volcanic Phase-3 was the last eruption phase in the early Danian beginning at the base of C29n, about 280,000 ky after the KTB mass extinction. Although this volcanic phase was much smaller than Phase-2, four of the longest lava flows occurred at this time (see Deccan volcanism website).
The onset of Deccan Phase-3 coincided with the extinction of the early Danian index species Parvularugoglobigerina eugubina and P. longiapertura. In the eastern Tethys, this volcanic event can be linked to a major negative d13C shift, similar to the KTB event (Magaritz et al., 1992), and Guembelitria blooms similar to the KTB event. In fact, when this event was first recognized in 1991 (Keller and Bejamini, 1991) it was thought to be the KTB event. The major high-stress conditions indicated by the Guembelitria blooms and d13C shift can no be correlated with Deccan Phase-3 volcanism (Fig. 9). The long delayed (500 ky) recovery of the marine ecosystem after the mass extinction may now be explained by the adverse environmental conditions as a result of Deccan volcanism.
Figure 9. Guembelitria blooms and d13C shift marks Deccan Phase-3 in the eastern Tethys. Adapted from Keller and Bejamini, 1991; Magaritz et al., 1992.
Abramovich, S., Keller, G., 2003. Planktonic foraminiferal response to the latest
Maastrichtian abrupt warm event: a case study from South Atlantic DSDP Site 525A. Mar. Micropaleontol. 48, 225â€“249.
Abramovich, S., Almogi-Labin, A.,Benjamini, Ch., 1998. Decline of the
Maastrichtian pelagic ecosystem based on planktic foraminifera
assemblage changes: Implication for the terminal Cretaceous faunal crisis.
Geology 26, 63-66.
Abramovich, S., Yovel-Corem, S., Almogi-Labin, A., Benjamini, C., 2010. Global
climate change and planktic foraminiferal response in the Maastrichtian.
Paleoceanography 25, PA2201.
Hess, S., Kuhnt, W., 1996, Deep-sea benthic foraminiferal recolonization of the
1991 Mt. Pinatubo ash layer in the South China Sea. Marine Micropaleontology 28, 171-197.
Keller, G., 2002. Guembelitria-dominated planktic foraminiferal assemblages
mimic early Danian in Central Egypt. Marine Micropaleontology 47, 71-99.
Keller, G., 2003. Biotic effects of impacts and volcanism. Earth and Planetary
Science Letters 215, 249-264.
Keller, G., 2005. Biotic effects of late Maastrichtian mantle plume volcanism:
implications for impacts and mass extinctions. Lithos, 79, 317-341.
Keller, G. and Abramovich, S., 2009. Lilliput Effect in late Maastrichtian
planktic Foraminifera: Response to Environmental Stress. Paleogeogr.,
Paleoclimatol., Paleoecol., 271, 52-68. doi:10.1016/j.palaeo.2008.09.007
Keller, G. and Benjamini, C., 1991. Paleoenvironment of the eastern Tethys in the early Danian, Palaios, 6: 439-464.
Keller, G., Pardo, A. 2004. Disaster opportunists Guembelitridae: index for environmental catastrophes. Marine Micropaleontology. 53, 83-116.
Keller, G., Adatte, T., Tantawy, A.A., Berner, Z., Stueben, D., 2007. High Stress
Late Cretaceous to early Danian paleoenvironment in the Neuquen Basin,
Argentina. Cretaceous Research, 28, 939-960.
Kucera, M., Malmgren, B.A., l998. Terminal Cretaceous warming event in the mid-latitude South Atlantic Ocean: evidence from poleward migration of Contusotruncana contusa (planktonic foraminifera) morphotypes. Palaeogeography, Palaeoclimatology, Palaeoecology 138, 1-15.
Li L., Keller, G., 1998a. Maastrichtian climate, productivity and faunal turnovers in
planktic foraminifera in South Atlantic DSDP Sites 525A and 21. Marine
Micropaleontology 33, 55-86.
Li L., Keller, G., 1998b. Abrupt deep-sea warming at the end of the Cretaceous.
Geology 26(11), 995-998.
Li L., Keller G., 1998c. Diversification and extinction in Campanian-Maastrichtian
planktic Foraminifera of northwestern Tunisia. Eclogae Geologicae
Helvetiae, 91(1), 75-102.
Magaritz, M., Benjamini, C., Keller, G., and Moshkovitz, S., 1992. Early
diagenetic isotopic signal at the Cretaceous-Tertiary boundary, Israel.
Palaeogeography, Paleaoclimatology, Palaeoecology 91, 191-304.
Olsson, R.K., Wright, J.D., Miller, K.D., 2001. Palobiogeography of Pseudotextularia elegans during the latest Maastrichtian global warming event. J. Foraminiferal Research 31, 275-282.