The longest delay: Re-emergence of coral reef ecosystems after the Late Devonian extinctions

Abstract

Reefs are an excellent tool for tracking marine-ecosystem changes, especially through mass extinction transitions. Although metazoan reefs proliferated during the Phanerozoic, prolonged metazoan reef-recovery intervals often occurred after extinction events. Here, we document and review the reef-recovery interval following the Late Devonian Frasnian-Famennian (Kellwasser) and end-Famennian (Hangenberg) mass extinctions, which eliminated the largest area of metazoan (stromatoporoid-coral) reefs of the Phanerozoic. Previous reports of the late Visean coral bioconstructions from western Palaeotethys Ocean, may mark the first metazoan reef proliferation after the Hangenberg extinction. In this study, abundant coral reefs, coral frameworks and coral biostromes were described in detail for the first time from the late Visean strata on the South China Block (eastern Palaeotethys Ocean). The occurrence of these coral bioconstructions further suggests that the late Visean coral reef recovery may have been a widespread phenomenon. Based on the high-resolution reef database constructed in this study, three sub-intervals of the Mississippian metazoan reef recovery were distinguished, which are (1) metazoan “reef gap” phase (MRG) without metazoan reefs during the Tournaisian; (2) metazoan reef re-establishment phase (MRR) containing a few metazoan reefs from early Visean to early part of the late Visean; and (3) metazoan reef proliferation phase (MRP) with global coral reef flourishment during the middle part of the late Visean (late Asbian to early Brigantian substages). Hence, coral reef ecosystems proliferated and became dominant in marine ecosystems during the late Asbian to early Brigantian, indicating a prolonged metazoan reef recovery of about 12 Ma and 23 Ma until the MRR and MRP, respectively. Coral reef proliferation at this time shows that the Mississippian was not solely a period dominated by microbial reefs. Late Visean coral reef development coincided with increased nektonic and benthic diversity, showing that metazoan reef recovery closely tracked overall marine ecosystem evolution. Even compared with other slow reef-recovery intervals, such as the middle-late Cambrian and Early-Middle Triassic with the intervals until the MRR and MRP of 5 Ma and 2 Ma, and 15 Ma and 9 Ma respectively, the Mississippian metazoan reef recovery was the longest in reef history. Harsh climatic and oceanic conditions were present during the Mississippian, mainly including the widespread marine anoxia during the middle part of Tournaisian and the following recurrent glacial and interglacial climatic episodes with frequent changes in sea level, sedimentary facies and sea-water surface temperature, which may have stymied metazoan reef recovery during this time. During the late Visean, marine communities flourished during a phase of relative warm conditions and high sea level, and coincided with the long-delayed re-emergence of coral reef ecosystems after the Late Devonian extinctions.

Introduction

Reefs typically form in shallow, tropical carbonate platforms, which are the cradle of evolution and sources of marine biodiversity (Kiessling et al., 2010). The earliest examples were formed of stromatolites and flourished during the Precambrian before declining in the Phanerozoic (Riding, 2006). Metazoan reefs first appeared in the late Ediacaran and proliferated during the Phanerozoic (Wood, 1999; Penny et al., 2014), albeit with time gaps after mass extinction events, which are often marked by microbial reef proliferation (Riding, 2006; Yao et al., 2016a).

The most persistent development of metazoan reef ecosystems occurred from the Ordovician to Devonian, when stromatoporoids and tabulate corals dominated (Copper, 2011; Zapalski et al., 2017a). It reached its climax during the Middle to Late Devonian (Givetian to Frasnian stages), when reefs covered about five million square kilometres (10 times the surface area of modern reef ecosystems) and had remarkable longitudinal extent (Copper, 1994; Copper and Scotese, 2003). This reef heyday was followed by the Famennian to Mississippian interval that saw the transition from Devonian greenhouse to Permo-Carboniferous icehouse climate (Montañez et al., 2011) and the Frasnian-Famennian (FF) Kellwasser and end-Famennian Hangenberg mass extinction events (Hallam and Wignall, 1997; Kaiser et al., 2016). The FF extinction caused the collapse of stromatoporoid-tabulate coral ecosystems, which were replaced by the early Famennian microbial reef ecosystems with a few stromatoporoid reefs (Copper, 2002). Then, the abundance of microbial and stromatoporoid reefs gradually declined until the latest Devonian when stromatoporoid reef ecosystems became dominant again only to be eliminated during the Hangenberg extinction (Webb, 2002; Yao et al., 2016a). The succeeding Mississippian has long been assumed to be an interval dominated by microbial reefs, containing a major metazoan “reef gap” (Heckel, 1974; Webb, 1994). Small-sized metazoan reefs gradually reappeared during the middle-late Mississippian (Visean Stage) (Webb, 2002; Aretz and Chevalier, 2007; Rodríguez et al., 2012; Yao and Wang, 2016). However, due to low-resolution and limited data available in previous studies (e.g. Webb, 2002), the timing and style of metazoan reef recovery in the Mississippian are unclear.

Evaluations of post-extinction marine ecosystems have focused primarily on the number of taxa, with less attention paid to ecological change (e.g., Poty, 1999; Song et al., 2011; Chen and Benton, 2012). However, biodiversity metrics do not reveal all aspects of recovery, and an ecological approach is essential (Chen and Benton, 2012; McGhee et al., 2013), particularly for metazoan reef ecosystems (Yao et al., 2016a). Metazoan reef recoveries after mass extinctions often occur following major time gaps, such as the middle-late Cambrian, Mississippian and Early-Middle Triassic (Lee et al., 2015; Yao et al., 2016a; Martindale et al., 2018). The longest metazoan “reef gap” was during the Mississippian (Adachi et al., 2015; Yao et al., 2016a), but the biodiversity variations in this interval are poorly documented, as are the coeval climatic and environmental changes. Thus, the trajectory of Mississippian marine ecosystem recovery after the Late Devonian mass extinctions requires more detailed study. Thus, our main aims are: 1) to review the Mississippian bioconstructions from the Palaeotethys and Panthalassa oceans and to describe the coeval coral bioconstructions in detail from the South China Block; 2) to reconstruct a global Mississippian reef database at a high temporal resolution in order to constrain the duration and timing of metazoan reef proliferation; 3) to compare the Mississippian metazoan reef evolutionary pattern with contemporaneous diversity changes in marine nektonic and benthic faunas, and thus provide insight into the overall marine ecosystem changes; and 4) to discuss the potential factors controlling the prolonged Mississippian metazoan reef recovery.