5.1. Paleoenvironmental Interpretation
In the Salinas Menores, rhodoliths are scattered in the marls, not concentrated in particular beds. The sediment trapped in the inner voids of the rhodoliths and that surrounding them show different micropaleontological content. Miliolids are very abundant in the sediment filling up the internal cavities of rhodoliths. These benthic foraminifers are typical inhabitants of protected lagoons as well as shallow inner-platform settings [44
]. However, the sediment engulfing the rhodoliths is rich in planktic foraminifers characteristic of deep environments. The micropaleontological content suggests that these rhodoliths are displaced from their original place of growth. The miliolids trapped within the rhodoliths when they were growing suggest that the algal nodules formed originally in a shallow platform. The abundance of members of the order Corallinales is typical of shallow water settings [47
]. Rhodoliths were afterwards transported to deeper basinal areas accumulating as allochthonous components. The presence of turbidites, channeled bodies, and olistoliths of varying sizes intercalated in the marls attests that downslope transport was common during the deposition of these materials.
The major biotic components of the middle Eocene carbonates in the Sierra del Zacatín are LBF (Figure 8
F). Coralline algae are present but as secondary representatives of the fossil assemblages. They occur mainly as crusts, attached to and intergrown with corals, and as rhodoliths, which are dispersed in the LBF-dominated carbonates. Algal crusts occur on top of coral colonies of varying sizes, indicating that colonies were preserved in their original growth position (Figure 8
B). In addition, geopetal structures infilling internal voids of rhodoliths indicate normal polarity. This is consistent with absence of substantial reworking or lateral displacements of the algal nodules.
In the lower Polo Unit in the southern Dominican Republic, spheroidal to ellipsoidal rhodoliths mainly composed of Hapalidiales and Sporolithales indicate relatively deep (several tens of meters) shelf environments [47
]. Abundant peyssonneliaceans are also characteristic of relatively deep shelf settings [56
]. The LBF associated to rhodoliths also suggests this kind of shelf environment [45
]. Lithofacies changes indicate deepening upwards in the succession [39
The rhodolith rudstones in the SJFB in northwestern Colombia probably formed in similar relatively deep-water, mesotrophic shelf environments [41
]. Foralgaliths of Hapalidiales and encrusting foraminifers are also characteristic of calm-water conditions [57
]. An increase of Hapalidiales and Peyssonneliaceans in red algal assemblages with depth was reported in the Priabonian of Austria [58
], late Eocene–late Oligocene in Northeast Italy [59
], and Miocene of Southern Spain [48
]. Rhodolith beds dominated by Hapalidiales and Peyssonneliaceans are generally recorded in middle-ramp settings in both modern [55
] and ancient depositional systems [4
The bed geometries, internal structures, and rip-up clasts clearly indicate that the packstones and rudstones intercalated in mudstones and siltstones in the SJFB are sediment gravity flow deposits [41
]. The rhodoliths in this lithofacies were removed from shallower shelf settings and redeposited in deeper marine environments in which the autochthonous sediments were mudstones and siltstones with planktic foraminifers. Bed geometry and dimensions indicate that these redeposited carbonates accumulated in small channel and lobe systems, downslope of the shelf in which rhodolith rudstones formed [41
]. The coralline algal composition does not differ significantly among rhodolith rudstones from mid-platform and those transported into deeper settings. This suggests that redeposited rhodoliths originally grew in the same middle platform paleoenvironments.
5.2. Taxonomic Composition
The studied rhodoliths are dominated by Hapalidiales and Sporolithales (Figure 9
A–D). Representatives of Corallinales are mostly limited to the pervasive presence of laminar thalli of Lithoporella
sp. and calcified segments of geniculates, except in Salinas Menores, where this order is relatively abundant and diverse (Figure 9
E,F). Extant species of the order Sporolithales are most diversified in relatively deep tropical waters [47
], although they also occur in shallow waters [70
]. Along the evolutionary history of the coralline algae, Sporolithales expanded worldwide and reached its highest diversification during the Upper Cretaceous, when greenhouse conditions prevailed. Afterwards, the species richness progressively decreased as the planet underwent a general decline in temperature [20
Hapalidiales, which outnumber other orders in coralline algal assemblages in modern cold, high-latitude waters and deeper low-latitude settings [47
], diversified during the Eocene, becoming more abundant than Sporolithales [20
]. As commented above, the Cenozoic decline in temperature started by the end of the early Eocene and accelerated at the end of this epoch with the onset of glaciation in Antarctica.
In terms of relative abundance, the coralline algal assemblages in mid-latitude Southern Spain and in the tropical Dominican Republic and Colombia show varying proportions of Sporolithales and Hapalidiales. The number of species belonging to these two groups varies in the different study areas (Table 1
). In Salinas Menores, Hapalidiales and Corallinales encompass higher species richness than Sporolithales (Table 1
). Complied data from the literature show that Hapalidiales started to diversify in the Ypresian (early Eocene) while Sporolithales slightly declined during the Eocene [20
]. Our data confirm the increasing replacement of Sporolithales by Hapalidiales during the greenhouse middle-Eocene.
The occurrence of Subterraniphyllum thomasii
in the Salinas Menores section is remarkable (Figure 9
G). This species was particularly abundant during Oligocene times, and some authors have considered it as a biostratigraphic indicator of this epoch (e.g., [71
]). Nonetheless, in the original description of the species, it is indicated that S. thomasii
also rarely occurs in late Eocene and Aquitanian (early Miocene) sediments [72
]. The presence of S. thomasii
in Salinas Menores extends back its occurrence to the Lutetian (lower middle Eocene).
is an extinct coralline alga characterized by laminar thalli with an isobilateral organization (Figure 9
H). D. biserialis
is particularly abundant in Paleocene and early Eocene carbonates and became gradually extinct during the Eocene [73
]. In the study areas, this species is virtually absent except for a few small fragments of thalli found in the Sierra del Zacatín, confirming its rarity in the middle Eocene (Table 1
5.3. Rhodolith Beds during the Eocene
Ecological factors required for the healthy development of rhodolith beds in recent oceans are well-oxygenated bottom conditions, low sedimentation rates, low content of suspended particles, and moderate water energy ([4
] and references therein). Except where rhodoliths were transported from shallower settings, rhodoliths in the rest of the study areas formed in oxygenated conditions, as shown by the prolific abundance of accompanying faunas, such as sea urchins, corals, LBF, bryozoans, and mollusks. In addition, carbonate sedimentation devoid of terrigenous particles indicates low sediment supply and, consequently, clear waters. Finally, absence of sedimentary structures suggests that turbulence was low to moderate.
Although local paleoenvironmental conditions were a priori favorable for rhodolith bed development, rhodoliths are major constituents in the study tropical middle Eocene shallow platform deposits, whereas LBF with varying proportions of calcareous red algae dominate in carbonate deposits at mid latitude. Similarly, Eocene deposits worldwide are mostly characterized by rhodoliths and coralline algal fragments dispersed in LBF-dominated carbonates, and the few examples of rhodolith beds were found so far in early or late Eocene (Figure 10
and Supplementary Material Table S2
). The low proportion of densely packed rhodolith beds during the Eocene, and particularly during the middle Eocene, coincides with a relative decline in algal diversity [20
] and with a significant decline in reef ecosystems [21
Nebelsick et al. [31
] performed a detailed facies analysis of middle Eocene to lower Oligocene ramp carbonates in different localities from Central and Southern Alps. Interestingly, coralline-algal-dominated facies (maerl, rhodolith, algal debris, and crustose algal facies) are frequent in upper Eocene and lower Oligocene deposits, while middle Eocene carbonate facies were largely dominated by LBF with subordinate algal debris and local rhodolith concentrations in middle ramp settings [31
Likewise, in several seamounts southeast of Japan, middle–late Eocene shallow water carbonates mainly dominated by LBF have been described [75
]. Coralline algae, forming rhodoliths or as fragments in rudstones to packstones, occur in lesser abundance. They became dominant afterwards, in Oligocene-to-Pleistocene carbonate deposits in the same western Pacific areas.
Profuse development of LBF mostly takes place in oligotrophic conditions [76
], although they can be also important in nutrient-rich tropical sediments in upwelling areas [80
]. Regarding coralline algae, it is not clear whether nutrient contents do actually promote the development of rhodolith beds. Present-day coralline algae withstand strong annual variations in nutrient conditions, from nearly depleted settings to high levels of nutrients (e.g., [81
]). However, it seems that profuse rhodolith beds mainly occur in mesotrophic conditions. The largest rhodolith beds in tropical latitudes occur nowadays on the eastern Brazilian shelf [84
], in areas with relatively reduced development of coral reefs [86
]. Here, rhodolith beds extend from shallow subtidal settings to the shelf margin [84
] and thrive under mesotrophic conditions, with mean seawater temperatures higher than 20 °C on the sea floor [88
], and low terrigenous sedimentation, which is generally limited to near-shore areas [91
]. Similarly, extensive rhodolith beds are found in the Amazon River mouth in the northwestern Brazilian platform, associated to the so-called Great Amazon Reef System [92
]. This is a complex of carbonate buildups including scleractinian corals, encrusting coralline algae, sponges, and rhodolith beds developed in the marginal areas of siliciclastic influx from the Amazon River under mesotrophic conditions [92
In subtropical latitudes in the Gulf of California, rhodoliths spread throughout the gulf [94
]. Nonetheless, large and dense rhodolith beds extend from shallow subtidal zone to about 40 m depth and occur in a wide spectrum of environmental conditions, with extreme variations of temperature (8–32 °C), and in mesotrophic waters in the middle part of the Gulf of California [81
]. Fine sediment input and related anoxia seem to be strong limiting factors for rhodolith development [94
In a similar way, the rhodolith beds in the Mediterranean occur in mesotrophic areas with reduced sedimentation and far from high nutrient influx [98
]. In the subtropical Western Pacific, on the shelves around the Ryukyu Islands, rhodolith beds develop; however, they do so in nutrient-poor waters lacking significant upwelling [54
The greenhouse conditions prevailing during great part of the Eocene favored the establishment of productive equatorial ocean waters and oligotrophic conditions widespread in middle and high latitudes [21
]. Paleoceanographic models as well as type of sediments show that productive upwelling zones were located in low latitudes, particularly in the Pacific, during the Eocene [77
]. Similarly, Boscolo-Galazzo et al. [104
] showed evidence of low nutrient conditions at mid-latitude in the southeastern Atlantic Ocean during the MECO. In our study cases, the middle Eocene deposits of the Chengue Formation in Colombia were formed in mesotrophic waters according to their micropaleontological content [41
]. We hypothesize that latitudinal gradient in oceanic productivity might account for the formation of rhodolith beds and rhodolith rudstone lithofacies in tropical areas, whereas LBF-enriched lithofacies prevailed in mid latitudes.
A precise reconstruction of environmental variables in middle Eocene carbonate records is difficult, which is generally true for Paleogene LBF- and coralline algal-dominated sediments. The impact of high temperatures due to high levels of atmospheric CO2
during the Eocene, and particularly during the hyperthermal events, on rhodolith bed development needs to be assessed. In this regard, sustained anomalously high summer temperatures led to high mortality rates of coralline algae in rhodolith communities along the western coast of Australia [105
]. In addition, and taking into consideration the discussion made above, the prevailing oligotrophic conditions at global scale accounting for the general prevalence of LBF during the middle Eocene and the relative decline of rhodolith beds worldwide requires further analyses. More calibration studies, essentially geochemical, for reconstructing water temperature and paleoproductivity, and knowledge of the depth habitats of benthic and planktic organisms are needed to define the multifactor settings that drove the carbonate grain associations found in low- and mid-latitude regions during the middle Eocene.