The Late Miocene Rifian corridor as a natural laboratory to explore a case of ichnofacies distribution in ancient gateways

Oceanic gateways have modulated ocean circulation and have influenced climatic variations throughout the Earth´s history. During the late Miocene (7.8–7.35 Ma), the Atlantic Ocean and the Mediterranean Sea were connected through the Rifian Corridor (Morocco). This gateway is one of the few examples of deep ancient seaways with a semi-continuous sedimentary record. Deposits comprise turbidites intercalated between deep-sea mudstone (i.e., hemipelagites and drift deposits), channelized sandstone contourite facies, and shallow marine sandstone. Herein an ichnological analysis was conducted in these upper Miocene sediments to improve characterisation of palaeoenvironmental conditions. In addition, ichnofacies were analysed to elucidate how bottom currents control ichnofacies distribution and can modify their attributes. Turbidite deposits are typified by vertical trace fossils (i.e., Ophiomorpha), conforming the Ophiomorpha rudis ichnosubfacies. Contouritic sandstone exhibits high density and low diversity trace-fossil assemblage, with predominant Macaronichnus and Scolicia, resembling a proximal expression of the Cruziana ichnofacies. Shallow marine environments are dominated by vertical trace fossils (e.g., Conichnus, Ophiomorpha, Skolithos), allowing an assignation to the Skolithos ichnofacies. This study reveals for the first time a variability in ichnofacies attributes and distribution at the Rifian Corridor, associated with turbidites, contourite and shallow marine sediments. Hydrodynamic energy reveals as the major factor controlling trace maker communities in the studied seaway. Highly energetic conditions typical of shallower settings are present in deeper-water environments (i.e., slope), contributing to ichnodiversity impoverishment in ichnofacies.

Oceanic gateways play a key role in controlling global ocean circulation and climate systems 1 . Ancient seaways are unique environments in which a complex interplay of processes may take place (i.e., oceanic-, tidal-, bottom-, turbiditic-and wind-currents) 2,3 . The constricted morphology of the seaway usually funnels and amplifies the currents that shape the seafloor (i.e., tidal currents) 4 . Previous sedimentological studies of ancient seaways have been largely focussed on shallow counterparts (generally between 100 and 150 m of water depth) [4][5][6] . Few published examples of deep ancient seaways (> 150 m) and associated deposits can be found. However, oceanographic studies have shown that deep seaways are different from shallow ones, with bottom-currents sometimes playing a dominant role [7][8][9] . The Rifian Corridor is one of those few examples ( Fig. 1) 2,3,10,11 .
During the late Miocene, the Atlantic Ocean and the Mediterranean Sea were connected by two principal gateways, with a complex morphology, sills and channels through south Iberia and north Africa -the Betic and Rifian corridors, respectively 12,13 . The Rifian Corridor was a main deep seaway of this network (Fig. 1). This gateway progressively closed (7.1-6.9 Ma) due to tectonically induced uplift, leading to the onset of the Mediterranean Salinity Crisis in the late Miocene 13,14 . During the late Tortonian, the seaway evolved into a narrow, deep corridor hosting a complex interplay of processes 2,3 .
Ichnological analysis comprises a wide range of tools (e.g., ichnofabric approach, ichnofacies model) that prove very useful in sedimentary basin research 15 . The ichnofacies model is of special interest for detailed palaeoenvironmental reconstructions and for recognizing, distinguishing, and interpreting sedimentary environments [16][17][18][19] . Recent steps in ichnological research have established means of recognising and characterising  www.nature.com/scientificreports/ contouritic processes, revealing the importance of ichnology as a proxy for discerning between contourites, turbidites, hemipelagites and pelagites 20-24 , but not without scepticism 25 . At any rate, the relationship between deep-sea settings and trace fossils is very complex, and depends highly upon the palaeonvironmental factors that affect trace makers 26 . Trace-fossil research on seaway environments has been conducted mainly on shallow marine settings, including brackish-water ecosystems (i.e., estuarine complexes, resulting in the so-called "brackish-water model" 27,28 ), beach-shoreface complexes with evidence of tidal processes 29,30 , and compound dune fields 31 . Still, detailed trace-fossil analysis and ichnofacies characterisation of ancient deep seaways has never been carried out. The aim of this research is to conduct a detailed ichnological analysis of selected outcrops of the Rifian Corridor (Ain Kansera, Sidi Chahed, Kirmta and Sidi Harazem), as a unique opportunity to assess trace-fossil variations to interpret an ancient deep-water seaway where shallow marine processes (i.e., tidal variations), pelagic/ hemipelagic settling, turbiditic supplies and contouritic flows closely (less than 20 km) interact 2,3 . We evaluate the importance of palaeoenvironmental factors such as nutrients, oxygenation, and flow velocity in a setting dominated by bottom currents, and their incidence on the trace maker community. The utility of the ichnofacies approach is underlined within the framework of improving high-resolution palaeoenvironmental reconstructions in different depositional environments of ancient deep gateways.
Trace-fossil assemblages at the Rifian Corridor. In both contouritic and turbiditic deposits, ichnodiversity is low (4 and 5 ichnogenera, respectively), whereas trace-fossil abundance is high in the former and moderate in the latter. Shallow marine deposits from the southern Rifian Corridor feature an abundant and moderately diverse trace-fossil assemblage (9 ichnogenera). Within the selected outcrops, the clear ichnological variability can be attributed to the different facies.
The Sidi Harazem turbiditic ichnoassemblage consists of 5 ichnogenera -Ophiomorpha (O. rudis), Planolites, Spirophyton, Thalassinoides, and Zoophycos ( Fig. 3E-H)-and the thick sandstone beds are more bioturbated than the marly ones. Ophiomorpha is the most abundant ichnogenus, and appears in the thick turbiditic sandstone beds; Thalassinoides is common, Planolites rare, and Zoophycos and Spirophyton is occasionally found. The trace-fossil assemblage of marly pelagic and hemipelagic deposits from the Sidi Harazem consists of abundant undifferentiated structures and scarce Planolites-like and Thalassinoides-like trace fossils.
The sandy contourites in Kirmta and Sidi Chahed comprise a highly abundant and scarcely diverse trace-fossil assemblage (4 ichnogenera), dominated by Macaronichnus and Scolicia, and common Planolites and Thalassinoides (Fig. 2). Trace fossils were predominantly found in the planar-stratified and cross-bedded sandstone. Turbidites show an absence of discrete trace fossils. The trace = fossil assemblage of muddy contourite deposits from both outcrops consist of regular undifferentiated biogenic structures and scarce Planolites-like and Thalassinoides-like trace fossils.

Ichnofacies characterisation. The trace-fossil assemblage of Sidi Harazem is typified by vertical burrows
of Ophiomorpha rudis and some Thalassinoides. Ophiomorpha is generally but not exclusively characteristic of high-energy environments (i.e., shoreface) in well-sorted, shifting sandy substrates, constituting a common element of the Skolithos and Cruziana ichnofacies 17,18 . However, the appearance of Ophiomorpha in deep-sea environments is also recorded, and usually explained as an effect of transport of the trace makers by currents from shallow marine environments into the deep-sea 33,34 . Uchman 35 proposed the Ophiomorpha rudis ichnosubfacies within the Nereites ichnofacies for the record of ichnoassemblages dominated by Ophiomorpha rudis in thick sandstone beds related with channels and proximal lobes in turbiditic systems 36 . Accordingly, the Sidi Harazem trace-fossil assemblage could be associated with the Ophiomorpha rudis ichnosubfacies. Ichnosubfacies/ichnofacies assignation is tentative due to the absence of other components of this ichnosubfacies (e.g., Scolicia, Nereites, graphoglyptids); this uncertainty is tied to outcrop limitations, e.g. the low exposure of turbiditic soles and difficulties in observing discrete trace fossils in the non-compact hemipelagic and pelagic deposits.
The trace-fossil assemblages of Kirmta and Sidi Chahed feature high abundance and low ichnodiversity, being dominated by horizontal trace fossils, such as Macaronichnus and Scolicia. Macaronichnus is usually interpreted as a shallow marine (up to foreshore) trace fossil 37 that occasionally appears in deeper water environments 38,39 and is commonly associated with the Skolithos ichnofacies [17][18][19]40 . Scolicia presents a wide environmental range, but is a typical element of the deep-marine Nereites and the shelfal Cruziana ichnofacies 40 . The proximal expression of the Cruziana ichnofacies is dominated by deposit-feeding burrows, but also includes structures of passive carnivores, omnivores, suspension feeders, as well as grazing forms 41 . This ichnofacies is defined as a transition between the distal expression of the Skolithos ichnofacies and the archetypal Cruziana ichnofacies 41 . The low ichnodiversity observed within the contourite facies from Kirmta and Sidi Chahed outcrops, together with the ubiquity of the dominant trace fossils, hamper a conclusive ichnofacies assignation. Still, though Macaronichnus is typical from high energy shallow marine environments, it may locally appear in the proximal Cruziana ichnofacies 41 . Considering the dominance of horizontal feeding trace fossils produced by deposit and detritus feeders over dwelling structures of suspension feeding structures, contourite ichnoassemblages at the Rifian    The trace-fossil assemblage of Ain Kansera is characterised by moderate ichnodiversity with a dominance of vertical (Skolithos and Ophiomorpha), cylindrical or conic-shaped (Conichnus) dwelling burrows of suspension feeders and passive predators. Horizontal trace fossils produced by a mobile fauna are scarce, mainly associated with Macaronichnus trace makers. According to these ichnological features, shallow marine facies at the Rifian Corridor -represented by Ain Kansera sediments-can be clearly assigned to the Skolithos ichnofacies, with predominant burrow systems having vertical, cylindrical, or U-shaped components of suspension feeders and passive predators, and a scarcity of horizontal trace fossils 17-19,40,42 . Ichnofacies in the Rifian Corridor seaways: hydrodynamic energy and the incidence of bottom currents. Over the past years, detailed ichnological research has revealed the major incidence of particular environmental factors (e.g., organic-matter content, oxygenation, sedimentation rate) on ichnological attributes from deep-sea environments, including ichnofacies characterisation and distribution 26 . The deep sea is a complex environment where several depositional processes co-exist, including pelagic/hemipelagic settling, bottom currents and gravity flows 9 . Trace-fossil analysis has proven useful for discerning and characterising such sedimentary environments and associated deposits 21 . Hydrodynamic conditions are a very significant limiting factor for trace makers, inducing variations in distribution and behaviour, hence in the preservation of trace fossils 19,29,43,44 . Typically, ichnoassemblages related to high energy conditions are characterised by vertical dwelling structures of infaunal suspension feeders and/or passive predators, forming low-diversity suites; ichnoassemblages related to low energy conditions are dominated by horizontal feeding trace fossils of deposit and detritus feeders, as well as higher diversity 19 . Ichnofacies identification is mainly based on the recognition of key features that connect biological structures with physical parameters (i.e., environmental conditions) [17][18][19] . Accordingly, ichnofacies reflect specific combinations of organisms´ responses to a wide range of environmental conditions.
In the case of seaways, prevailing hydrodynamic conditions are a main environmental factor, along with controlling depositional processes and sedimentation regimes 6,30 . Even though the number of trace-fossil studies is considerably lower than in other clastic shallow or deep marine environments, ichnological analysis has proven to be useful to characterise waves, tides or storms in shallow seaways 29,30 , overlooking deep seaways and their implications. Deep seaways with narrow palaeogeographical configuration, as is the case of the Rifian Corridor 10 , would promote higher energetic conditions than those typical of deep-sea environments. In the study area, clearly distinct sedimentary environments -in terms of hydrodynamic conditions, bathymetry, rate of sedimentation, etc.-are closely spaced 2 , passing from shallow marine to turbiditic slope systems in less than 20 km (Fig. 4). Such variations in palaeoenvironmental conditions are supported by ichnofacies characterisation and distribution.
Turbidite deposits from Sidi Harazem, emplaced on the slope of the Rifian Corridor, are typified by vertical trace fossils, mainly by the record of Ophiomorpha rudis. These ichnological attributes are similar to those associated with particular sub-environments (e.g., channels and proximal trubiditic lobes) of the turbiditic systems, conforming the Ophiomorpha rudis ichnosubfacies inside the Nereites ichnofacies 36 .
Sandy contourite 2D-and 3D-dune facies (upper slope environment) (Fig. 4) from Sidi Chahed and Kirmta are related to high-energy deep-water environments. However, they are dominated by horizontal trace fossils (Macaronichnus and Scolicia) produced by mobile deposit-and detritus-feeders, discarding a direct assignation to the Skolithos ichnofacies. In this case, palaeoenvironmental conditions other than hydrodynamic energy must be considered to explain the dominance of horizontal forms and the absence of vertical biogenic structures. The record of densely Macaronichnus ichnoasemblages in these contourite sediments was recently linked to high nutrient supply provided by ancient bottom currents 39,45 . This agrees with the record of Scolicia: its abundance and size usually increase in conjunction with greater amounts and nutritious values of benthic food 20,46 . Thus, the strong palaeo-MOW bottom currents that dominated the slope may have created well-oxygenated and nutrientrich benthic environments, favouring colonisation by trace makers that could exploit such accumulations of organic matter inside the sediment. Macaronichnus and Scolicia producers could develop an opportunistic behaviour, determining rapid and complete bioturbation, avoiding colonisation by other trace makers -including suspension feeders-these ichnological features resemble the Cruziana ichnofacies attributes. Notwithstanding, the high ichnodiversity that is characteristic of the Cruziana ichnofacies is absent here. The great abundance and low ichnodiversity observed for the contourite facies appear to indicate the absence of an archetypal Cruziana ichnofacies, but the development of the proximal Cruziana ichnofacies. Bottom currents and their associated deposits (i.e., contourites) have been previously linked to both the Cruziana and Zoophycos ichnofacies in Cyprus Miocene carbonate contourite deposits 22,23 , meaning that contourite deposits are not exclusively related to a single ichnofacies. The replacement from the Zoophycos to Cruziana ichnofacies was interpreted to be mainly controlled by sea level dynamics 23 .
The shallow marine facies from Ain Kansera (shoreface environment) are dominated by vertical, cylindrical, or U-shaped dwelling burrows (Conichnus, Ophiomorpha and Skolithos) of suspension feeders (Fig. 4). These attributes are usually related to high energetic conditions developed in shallow marine environments conforming the Skolithos ichnofacies 18 .
In short, at the Rifian Corridor, ichnofacies distributions from proximal to distal settings are controlled by bottom currents (palaeo-MOW), with hydrodynamic conditions being the major palaeonvironmental limiting factor. Particularly noteworthy is the development of the proximal Cruziana ichnofacies in deeper settings from the slope environments; bottom currents generated high energetic conditions similar to those of shallow/ proximal areas.

Geological setting. The Rifian Corridor (Morocco) connected the Atlantic Ocean and the Mediterranean
Sea during the late Miocene (Fig. 1). The outcrops studied herein are located on the northern flank of the Saiss Basin in the South Rifian Corridor, west of Taza-sill 10 (Fig. 1). This basin comprises middle to upper Miocene foreland deposits 32 and records a unique contourite channel system related to the palaeo-Mediterranean Outflow Water (Palaeo-MOW 2 ), which resulted from net evaporation in the Mediterranean leading to dense water formation. Regional tectonic activity favoured the development of turbiditic and gravity flows, inducing a complex deep system in which variable sedimentary processes interacted 2 . Four outcrops (Fig. 1)   www.nature.com/scientificreports/ and composed of poorly to moderately sorted, medium-to coarse-grained sand. Locally, channel-like features are observed. The deposits have been associated to a basinal turbidite system with benthic foraminiferal assemblages indicating water depths of 250-400 m 10 . The Sidi Chahed sections, previously studied by Capella et al. 10 and de Weger et al. 2 , and the Kirmta outcrop, previously studied by de Weger et al. 2 , consist of three main channelized upper Tortonian (7.8-7. 51 Ma) sandstone units encased in blue marls. Both outcrops contain different orders of unidirectional traction structures, ranging from ripples to m-scale 3D-dunes. Interbedded slump deposits have been identified within the main sandstone bodies, while turbidites have been recognized between the main sandstone bodies that are encased by marlstones 2 . In both outcrops, the blue marls have been most likely interpreted as muddy contourites (see Capella et al. 10 and de Weger et al. 2 ). Both outcrops were deposited within a palaeodepth range from the upper slope to the outer shelf (150-400 m water depth) 2,10 .
The Ain Kansera outcrop consists of upper Tortonian (between 7.51 and 7.31 Ma) sandstone and marlstone intercalations 10 . Sandstone bed thicknesses range from 1 to 10 m, the beds containing medium-to coarse-and very coarse-grained sand. They consist of a compositional mix of siliciclastic and bioclastic sand, and regularly contain hummocky and swaley cross-stratification. Benthic foraminiferal assemblages and the presence of hummocky cross-stratification indicate an inner shelf environment (water depths of 50-100 m) 10 . Toward the top, the thick sandstone intervals probably represent a shallower (15-50 m water depth) wave-dominated infralittoral setting.
Methodology. Ichnological analysis from the selected sections at Sidi Harazem (50 m), Sidi Chahed (130 m), Kirmta (70 m) and Ain Kansera (50 m) was conducted first at the outcrop and then in laboratory. Special attention was pay to the correlation between ichnological attributes, facies and bed features (preservation within sedimentary beds and relationship with bottom and top surfaces). Outcrop analysis was performed bed-by-bed focusing on abundance, diversity and macroscopic morphological burrow features (e.g., orientation, shape, length/diameter, cross-cutting relationships, and taphonomy). Collected specimens were examined in the laboratory under microscope, with special attention to ichnotaxonomical features (e.g., infilling material, burrow wall). The images of some photographed specimens (outcrop and laboratory) were treated with image software to improve visibility of ichnological features 47 . Collected samples are housed in the Department of Stratigraphy and Palaeontology, University of Granada.

Data availability
All data analysed in this study are summarised in this published article. The original datasets are not publicly available due to size restrictions, but are available from the corresponding author upon request.