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