The evolution of mid Paleocene-early Eocene coral communities: How to survive during rapid global warming

https://doi.org/10.1016/j.palaeo.2011.12.010Get rights and content

Abstract

Today, diverse communities of zooxanthellate corals thrive, but do not build reef, under a wide range of environmental conditions. In these settings they inhabit natural bottom communities, sometimes forming patch-reefs, coral carpets and knobs. Episodes in the fossil record, characterized by limited coral-reef development but widespread occurrence of coral-bearing carbonates, may represent the fossil analogs of these non-reef building, zooxanthellate coral communities. If so, the study of these corals could have valuable implications for paleoenvironmental reconstructions. Here we focus on the evolution of early Paleogene corals as a fossil example of coral communities mainly composed by zooxanthellate corals (or likely zooxanthellate), commonly occurring within carbonate biofacies and with relatively high diversity but with a limited bioconstructional potential as testified by the reduced record of coral reefs. We correlate changes of bioconstructional potential and community compositions of these fossil corals with the main ecological/environmental conditions at that time. The early Paleogene greenhouse climate was characterized by relatively short pulses of warming with the most prominent occurring at the Paleocene-Eocene boundary (PETM event), associated with high weathering rates, nutrient fluxes, and pCO2 levels. A synthesis of coral occurrences integrated with our data from the Adriatic Carbonate Platform (SW Slovenia) and the Minervois region (SW France), provides evidence for temporal changes in the reef-building capacity of corals associated with a shift in community composition toward forms adapted to tolerate deteriorating sea-water conditions. During the middle Paleocene coral–algal patch reefs and barrier reefs occurred from shallow-water settings, locally with reef-crest structures. A first shift can be traced from middle Paleocene to late Paleocene, with small coral–algal patch reefs and coral-bearing mounds development in shallow to intermediate water depths. In these mounds corals were highly subordinated as bioconstructors to other groups tolerant to higher levels of trophic resources (calcareous red algae, encrusting foraminifera, microbes, and sponges). A second shift occurred at the onset of the early Eocene with a further reduction of coral framework-building capacity. These coral communities mainly formed knobs in shallow-water, turbid settings associated with abundant foraminiferal deposits. We suggest that environmental conditions other than high temperature determined a combination of interrelated stressors that limited the coral-reef construction. A continuous enhancement of sediment load/nutrients combined with geochemical changes of ocean waters likely displaced corals as the main bioconstructors during the late Paleocene-early Eocene times. Nonetheless, these conditions did not affect the capacity of some corals to colonize the substrate, maintain biodiversity, and act as locally important carbonate-sediment producers, suggesting broad environmental tolerance limits of various species of corals. The implications of this study include clues as to how both ancient and modern zooxanthellate corals could respond to changing climate.

Highlights

► Mid Paleocene-Early Eocene zooxanthellate corals with reef-building potential. ► Multi-step evolution of corals with progressive reduction of reef-building potential. ► Shift towards thermal stress- and high turbidity/nutrients-tolerant communities. ► Expansion of non-reef building corals related to ocean chemistry perturbations.

Introduction

Diverse coral communities dominated by different kinds of zooxanthellate, colonial forms, occur today in a broad range of marine settings where temperature, nutrients, light levels, and aragonite saturation fluctuate or remain close to what are considered thresholds for coral survival (e.g., Kleypas et al., 1999). In these sites zooxanthellate coral assemblages with constructional potential are developed with a composition comparable to that of coral reefs, however, they do not form a framework. These assemblages are often characterized by high species richness and represent localized sites of carbonate sediment production and accumulation (e.g., Benzoni et al., 2003, Moyer et al., 2003, Perry, 2003, Perry and Larcombe, 2003, Riegl, 2003, Halfar et al., 2005, Thomson and Frisch, 2010). These examples highlight the necessity for a distinction between reef-building versus non reef-building corals as compared with symbiont bearing (zooxanthellate, z-corals) and non-symbiont bearing (azooxanthellate corals, az-corals). Corals are traditionally categorized as either hermatypic (reef building) or ahermatypic (non reef building), which is often treated as being equivalent to zooxanthellate versus azooxanthellate. However, many kinds of both z- and az-corals can build reefs only if the environment supports minimal deposition (e.g., Hallock, 1988). Therefore, reef-building capacity is not necessary correlated to algal symbiosis. Hosting zooxanthellae does not translate into reef building if the environmental conditions do not support hypercalcification and/or if the nutrient regime supports bioerosion rates that exceed deposition rates (e.g., Pomar and Hallock, 2008). Similarly, diversity and reef-building capacity are not necessary correlated (as demonstrated for example by Johnson et al., 2008). If environmental conditions are conducive to either hypercalcification or to minimal deposition, just a few species or even a single species can build a carbonate mound or even a reef (e.g., Porites-reefs during the Miocene, Pomar, 1991; modern Porites reefs in east-central tropical Pacific, e.g., Cortés, 1997).

In this study we focus on the evolution of early Paleogene zooxanthellate corals (or zooxanthellate-like corals, for forms resembling modern zooxanthellate corals see Rosen and Turnšek, 1989), as a possible fossil analogs of these modern non-reef building, zooxanthellate coral communities. The early Paleogene fossil record is characterized by a lack of extensive coral reefs, although coral facies, dominated by z- and z-like forms, have been reported commonly in shallow neritic facies (e.g., Drobne et al., 1988, Schuster, 1996, Baceta et al., 2005, Zamagni et al., 2009). These coral assemblages were characterized by constructional potential but a general limited reef-building capacity.

The early Paleogene experienced the most pronounced long-term warming of the Cenozoic, starting in the late Paleocene (~ 59 Ma) and culminating in the early Eocene (~ 51 Ma) with the Early Eocene Climatic Optimum (EECO; Zachos et al., 2001). Short-term warming events, known as hyperthermals, were superimposed on this long-term warming trend, including most notably the Paleocene-Eocene Thermal Maximum (PETM or ETM-1, Kennett and Stott, 1991), the ETM-2 or “Elmo” event, (Lourens et al., 2005), and the ETM-3 or “X” event (Agnini et al., 2009). These hyperthermals are characterized by carbonate dissolution horizons and negative carbon isotope excursions (CIE) (Lourens et al., 2005, Zachos et al., 2005, Nicolo et al., 2007, Zachos et al., 2010). They are likely related to abrupt and massive releases of 13C-depleted carbon into the ocean–atmosphere system (Dickens et al., 1995). The onset of the PETM was characterized by rapid changes in terrestrial and marine biota, including the largest extinction of benthic foraminifera (~ 40% of the species, e.g., Thomas, 2007) recorded during the Cenozoic. Pelagic ecosystems showed rapid diversification with high origination and extinction levels in planktonic foraminifera and calcareous nannofossils (e.g. Kelly et al., 1998, Kelly, 2002, Bralower, 2002, Gibbs et al., 2006). On shallow-water carbonate platforms, the rapid diversification of larger benthic foraminifera has been related to the PETM (Orue-Etxebarria et al., 2001, Scheibner et al., 2005). A causal link between the decreased volume of coral reefs and the global warming events of the late Paleocene-early Eocene time interval , particularly the PETM, has been frequently suggested (Scheibner and Speijer, 2008a, Scheibner and Speijer, 2008b), based on comparison with modern coral reef system responses to ongoing increase of sea-water temperature. Such an actualistic approach is not fully convincing, because what is happening today is much more than bleaching, and includes increasing temperature, ocean acidification, nutrient loading, increased (and increased variability in) short-wavelength radiation caused by stratospheric ozone depletion and coastal development (i.e., fluctuating delivery of photo-protective tannins to coastal waters), transport of microbes worldwide (e.g., Hallock, 2005 and references therein). A major difference is that modern perturbations are not occurring in an ocean with high calcium concentrations (e.g., Pomar and Hallock, 2008). Finally, there are great differences between modern and early Paleogene coral assemblages. For instance, Acropora-dominated communities that greatly promote the rate of modern reef growth are a relatively recent “invention” (Veron, 2000) with Acropora-dominated assemblages virtually absent until the end of the Early Miocene (McCall et al., 1994). These assemblages can be hardly compared with any of the early Paleogene coral communities. However, since the 1970s, acroporid species in the Caribbean have experienced extreme and accelerating declines estimated at 90–98% (e.g., Aronson and Precht, 2001). Modern Caribbean might represent a relatively good model for the Tethys in the early Paleogene.

The reduced reef-building potential of early Paleogene z-corals (Scheibner and Speijer, 2008b), not mirrored by a decline of diversity (e.g., Rosen, 2000), and the nature of these communities that survived the most intense global warming event of the last 50 My, deserve a more detailed study. To tackle this issue we critically screened and synthesized the published literature with the aim to document the main features and changes characterizing the coral assemblages throughout the mid Paleocene-early Eocene time span and to investigate the possible responses to rapid and frequent environmental changes. These questions have been addressed during our study of coral communities from the Adriatic Carbonate Platform (SW Slovenia), where unexpected diverse coral assemblages characterized late Paleocene microbialite-coral mounds (Zamagni et al., 2009), and from the Minervois region (SW France), where early Eocene diverse non-reef building coral assemblages thrived in deltaic, turbiditic shallow-water settings (Zamagni and Mutti, 2007). Based on the present study, we suggest that the evolution of these early Paleogene corals was a multi-step process triggered by the progressive expansion of shallow-water settings characterized by enhanced nutrients and sediment load associated with unfavorable seawater composition (mainly acidification of shallow waters). These conditions might have reduced coral calcification rates limiting their possibility to build permanent reef structures. Nonetheless, coral assemblages maintained relatively high diversity and shifted toward assemblages dominated by sediment/nutrient tolerant forms.

Section snippets

Terminologies

Numerous definitions of coral reefs, reef frameworks, reef communities exist in the literature (for a review of terminology see, for example, Riegl and Piller, 2000). According to Riegl and Piller (2000), the term reef is used in this work to describe the development of three-dimensional, biologically influenced buildups of coral framework and carbonate sediments. The use of the term framework follows Fagerstrom (1987) as denoting a mass of colonial, intergrown skeletal organisms. A further

The early Paleogene and the late Cretaceous corals: something in common

The long-term comparison between coral-reef accretion and coral diversity based on the data from Kiessling and Baron-Szabo (2004) shows that two parameters are closely correlated for all epochs except for the late Cretaceous to late Paleocene-early Eocene interval. During that interval this relationship appears to be reversed, with a clear decoupling between diversification of corals and coral-reef construction (Fig. 1). After the K–T crisis, which caused ~ 30% generic extinction of corals (

Material and methods

To tackle the issue of the evolution of the early Paleogene coral fossil community, we collected a broad database from the Tethys, the Atlantic, and the Caribbean realms from low- to mid-latitude carbonate settings. The earliest Paleocene is characterized by a gap in the fossil record of coral reefs, with the occurrences of early Danian corals represented by azooxanthellate forms from high latitudes (Kiessling and Baron-Szabo, 2004), and thus is not included in this work. After screening the

Results: evolution of mid Paleocene-early Eocene coral communities

Even with the uncertainties described above, Fig. 2 highlights some trends in the evolution of early Paleogene coral assemblages (Table 3). The middle Paleocene (Table 1) was a time when corals dominated the reef community (67% of the coral occurrences, Table 3), producing mainly patch-reefs in shallow-water settings but also reef complexes (Fig. 3a). In the frame of the low-level diversity of earliest Paleogene corals, the middle Paleocene coral assemblages can be considered moderately diverse

Diversity trends in early Paleogene shallow-water biocalcifiers

During the late Paleocene to early Eocene, other groups of phototrophic marine organisms underwent rapid radiations. An overview of the evolution of these biocalcifiers can help to better understand the paleoecology of the early Paleogene coral communities. The Paleocene shallow-water benthic communities where characterized by a rapid diversification of calcareous algae (Fig. 4). Starting from the Maastrichtian across the whole Paleocene and the early Eocene, calcareous coralline algae expanded

Conclusions

  • Analysis of coral occurrences during the early Paleogene show that the evolution of these coral communities was characterized by a progressive reduction of reef-building potential. In particular, 1) the mid Paleocene record was dominated by shallow-water coral–algal patch-reefs/reef complexes (67%), 2) the late Paleocene record was characterized by small shallow-water coral–algal patch-reefs (43%) together with coral-bearing mounds at shallow and intermediate depths (43%) where corals are

Acknowledgments

We thank the German Science Foundation (DFG project MU1680/7-1), the IAS and the Graduate School of the University of Potsdam for the grants awarded to Jessica Zamagni. We are grateful to Wolfgang Kiessling and Paolo Ballato for their help, fruitful discussions, and comments, as we are particularly grateful to Dragica Turnšek for the help and assistance with coral determinations. Taylor F. Schildgen and Carly Osborne are thanked for valuable improvement of English. We would like to thank two

References (155)

  • J.B. Lough et al.

    Environmental controls on growth of the massive coral Porites

    Journal of Experimental Marine Biology and Ecology

    (2000)
  • X. Orue-Etxebarria et al.

    Did the Late Paleocene Thermal Maximum affect the evolution of larger foraminifers? Evidence from calcareous plankton of the Campo Section (Pyrenees, Spain)

    Marine Micropaleontology

    (2001)
  • N. Özgen-Erdem et al.

    Benthic foraminiferal assemblages and microfacies analysis of Paleocene-Eocene carbonate rocks in the Kastamonu region, Northern Turkey

    Journal of Asian Earth Sciences

    (2005)
  • D. Abrego et al.

    Species specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress

    Proceedings of the Royal Society of London

    (2008)
  • G. Accordi et al.

    Depositional history of a Paleogene carbonate ramp (Western Cephalonia, Ionian Islands, Greece)

    Geologica Romana

    (1998)
  • G. Accordi et al.

    Biostratigraphy and facies analysis of the Jatibungkus olistolith (Central Java)

  • C. Agnini et al.

    An early Eocene carbon cycle perturbation at similar to 52.5 Ma in the Southern Alps: chronology and biotic response

    Paleoceanography

    (2009)
  • J. Aguirre et al.

    Dasycladalean algal biodiversity compared with global variations in temperature and sea level over the Past 350 Myr

    Palaios

    (2005)
  • J. Aguirre et al.

    Diversity of coralline red algae: origination and extinction patterns from the early Cretaceous to the Pleistocene

    Paleobiology

    (2000)
  • R.B. Aronson et al.

    White-band disease and the changing face of Caribbean coral reefs

    Hydrobiologia

    (2001)
  • B. Bagherpoura et al.

    Facies, paleoenvironment, carbonate platform and facies changes across Paleocene Eocene of the Taleh Zang Formation in the Zagros Basin, SW Iran

    Historical Biology

    (2011)
  • R. Baron-Szabo

    Austrian Scleractinian corals from the K/T-boundary to the Miocene

    Berichte des Institutes für Erdwissenschaften, Karl-Franzens-Universität Graz

    (2004)
  • R.C. Baron-Szabo

    Coral of the K/T-boundary: scleractinian corals on the suborders Astrocoeniiina, Faviina, Rhipidogyrina and Amphiastraeina

    Journal of Systematic Paleontology

    (2006)
  • S. Bentov et al.

    The impact of biomineralization processes on the Mg content of foraminiferal shells: a biological perspective

    Geochemistry, Geophysics, Geosystems

    (2006)
  • F. Benzoni et al.

    Coral communities of the northwestern Gulf of Aden (Yemen): variation in framework building related to environmental factors and biotic conditions

    Coral Reefs

    (2003)
  • R. Berkelmans et al.

    The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change

    Proceedings of the Royal Society of London Biological Sciences

    (2006)
  • M. Bernecker

    Biotic response to sea-level fluctuations and climate change: a case study from the Paleogene shelf of Oman

  • F. Bosellini

    Diversity, composition and structure of Late Eocene shelf-edge coral associations (Nago Limestone, Northern Italy)

    Facies

    (1998)
  • T.J. Bralower

    Evidence of surface water oligotrophy during the Paleocene–Eocene Thermal Maximum: nannofossil assemblage data from the Ocean Drilling Program Site 690, Maud Rise, Weddell Sea

    Paleoceanography

    (2002)
  • B.E. Brown

    Coral bleaching: causes and consequences

    Coral Reefs

    (1997)
  • J.R. Bryan

    A Paleocene coral–algal-sponge reef from southwestern Alabama and the ecology of Early Tertiary reefs

    Lethaia

    (1991)
  • J.R. Bryan et al.

    The Salt Mountain Limestone of Alabama

    Tulane Studies in Geology and Paleontology

    (1997)
  • F.A. Budd

    Diversity and extinction in the Cenozoic history of Caribbean reefs

    Coral Reefs

    (2000)
  • W.-J. Cai et al.

    Acidification of subsurface coastal waters enhanced by eutrophication

    Nature Geoscience

    (2011)
  • F. Carbone et al.

    Facies analysis and biostratigraphy of the Auradu Limestone Formation in the Berbera–Sheikh Area, northwestern Somalia

    Geologica Romana

    (1993)
  • J. Cortés

    Biology and geology of eastern Pacific coral reefs

    Coral Reefs

    (1997)
  • E.M. Crouch et al.

    Late Paleocene-early Eocene dinoflagellate cyst records from the Tethys: further observations on the global distribution of Apectodinium

  • H. Daod

    Carbonate microfacies analysis of Sinjar formation from Qara Dagh Mountains, South-West of Sulaimani City, Kurdistan region, Iraq

    World Academy of Science, Engineering and Technology

    (2009)
  • G.R. Dickens et al.

    Dissociation of oceanic methane hydrates as a cause of the carbon isotope excursion at the end of the Paleocene

    Paleoceanography

    (1995)
  • K. Drobne et al.

    Maastrichtian, Danian and Thanetian beds in Dolenja Vas (NW Dinarides, Yugoslavia). Mikrofacies, foraminifers, rudists and corals

    Razprave

    (1988)
  • J.M. Dupont et al.

    A retrospective analysis and comparative study of stony coral assemblages in Biscayne National Park (1977–2000)

    Journal of Caribbean Research

    (2008)
  • E.N. Edinger et al.

    Oligocene-Miocene extinction and geographic restriction of Caribbean corals; roles of turbidity, temperature, and nutrients

    Palaios

    (1994)
  • H. Eichenseer et al.

    The marine Paleogene of the Tremp region (NE Spain)—depositional sequences, facies history, biostratigraphy and controlling factors

    Facies

    (1992)
  • J. Erez

    The source of ions for biomineralization in foraminifera and their implications for paleoceanographic proxies

    Reviews in Mineralogy and Geochemistry

    (2003)
  • A.G. Fagerstrom

    The Evolution of Reef Communities

    (1987)
  • S.H. Frost et al.
  • S.J. Gibbs et al.

    Nannoplankton extinction and origination across the Paleocene–Eocene Thermal Maximum

    Science

    (2006)
  • L. Giusberti et al.

    Mode and tempo of the Paleocene Eocene thermal maximum in an expanded section from the Venetian pre-Alps

    Geological Society of America Bulletin

    (2007)
  • S. Grötz

    Biotic interaction and synecology in a Late Cretaceous coral–rudist biostrome of southeastern Spain

    Palaeogeography, Palaeoclimatology, Palaeoecology

    (2003)
  • J. Halfar et al.

    Nutrient and temperature controls on modern carbonate production: an example from the Gulf of California, Mexico

    Geology

    (2004)
  • Cited by (42)

    • A coral hotspot from a hot past: The EECO and post-EECO rich reef coral fauna from Friuli (Eocene, NE Italy)

      2022, Palaeogeography, Palaeoclimatology, Palaeoecology
      Citation Excerpt :

      By comparison with the available literature and database, this fauna represents the oldest high diversity assemblage ever reported after the K-Pg extinction event with values, especially during the post-EECO 2 interval, also higher than those of the Oligocene when luxuriant coral reefs emerged at the global scale (Budd, 2000; Bosellini et al., 2021). If we compare our data for genus richness with those available from our PalEoCoral database and from the PBDB database and we place them in the palaeogeographic map of the early Eocene (Fig. 12), we can actually see that, during the Ypresian, colonial scleractinian corals were actually concentrated in the central Neotethys (Kühn, 1966; Košir, 1997; Vecsei and Moussavian, 1997; Baron-Szabo, 2004; Turnšek and Košir, 2004; Kleeman, 2009; Zamagni et al., 2012; Accordi et al., 2014; Giusberti et al., 2014; Vescogni et al., 2016; Bosellini et al., 2020) and subordinately from western (Eichenseer and Luterbacher, 1992; Ferratges et al., 2021) southern (Schuster, 1998) and easternmost (Nuttall, 1932; Carbone et al., 1993; Bernecker, 2005; Jauhri et al., 2006) parts of the Neotethyan realm. Only a few genera have been reported from isolated localities of New Zealand (Campbell et al., 1993), North (Durham, 1942; Squires and Goedert, 1994; Vaughan, 1941; Toulmin, 1977) and Central (Frost and Langenheim, 1974; Budd, 2000) America, and Africa (Herbig, 1986; Trappe, 1991).

    • Unravelling the distribution of decapod crustaceans in the Lower Eocene coral reef mounds of NE Spain (Tremp-Graus Basin, southern Pyrenees)

      2021, Palaeogeography, Palaeoclimatology, Palaeoecology
      Citation Excerpt :

      In a well-documented case study, the peak of decapod diversity in Albian reefs of the southwestern Pyrenean domain correlated with ecological factors, and was not a preservational artefact (Klompmaker et al., 2013a). The coralgal reef record around the Paleocene-Eocene transition is scarce, and is dominated by isolated reefs, subordinate to other buildups dominated by calcareous algae and large benthic foraminifera (Rasser et al., 2005; Zamagni et al., 2012; Scheibner and Speijer, 2008; Vescogni et al., 2016). Following the Paleocene-Eocene Thermal Maximum (PETM), the Eocene was a critical epoch in the development of many modern-day features of the Earth, for example palaeogeographical configurations, ocean circulation patterns and several climatic conditions (e.g., Hallock et al., 1991; Hallock and Pomar, 2008; Stickley et al., 2009).

    View all citing articles on Scopus
    View full text