Early Cretaceous shifting of Zoophycos in the Ouarsenis Mountains (northwestern Algeria)

Ima Bouchemla , Li-Jun Zhang , Maani Benyoucef ,Mariusz A.Salamon

a Department of Geological Sciences, Faculty of Biological and Agricultural Sciences, Mouloud Mammeri University of Tizi-Ouzou, P.O.Box.17, DZ-15000 Tizi-Ouzou, Algeria

b Laboratoire de G′eomatique, ′Ecologie et Environnement, Mustapha Stambouli-Mascara University,DZ-29000 Mascara, Algeria

c School of Resources and Environment, Henan International Joint Laboratory of Biogenic Traces and Sedimentary Minerals, Henan Polytechnic University, Jiaozuo 454003, Henan Province, China

d Institute of Earth Sciences, University of Silesia in Katowice, B?dzi′nska 60, 41-200 Sosnowiec, Poland

Abstract Early Cretaceous succession of the Oued Fodda Formation in the Ouarsenis Mountains (northwestern Algeria)is mainly composed of marl－limestone alternations, which are subdivided into four informal units (Units 1 to 4), based on distinct lithological, stratonomical, and ichnological features.The ichnological analysis reveals a low diversity of the trace-fossil assemblage,which is exclusively reported from Units 2 and 3.The ichnoassemblage contains six ichnotaxa (Chondrites intricatus, Ophiomorpha isp., Planolites isp., Thalassinoides isp.,Zoophycos brianteus,and Zoophycos cauda-galli),among which Zoophycos and Chondrites are the most common elements of the assemblage and occur in distinct mud-rich substrates showing different bioturbation intensities.The development of Zoophycos in the middle part of Unit 2 shows a high degree of bioturbation(bioturbation index(BI)=4).Zoophycos specimens are of large size,between 45 cm and 75 cm in width,which were interpreted to have formed in a lower offshore environment where the oxygenation amount was optimal,the sedimentation rate was low,and the benthic food was abundant on the seafloor.Toward the upper part of Unit 2,Zoophycos-bearing levels exhibit a less intense degree of bioturbation(BI between 1 and 2)in contrast to Planolites-and Chondrites-bearing levels which have a bioturbation index(BI)between 3 and 4.At these levels, Zoophycos displays relatively small, coiled to U-shaped spreiten, probably in response to stressful and dysoxic conditions prevailing in the water bottom.With improved oxygenation in a quiet lower offshore to shelf margin environment in Unit 3,the benthic organisms recovered,as represented by medium to large size Zoophycos in association with Ophiomorpha and scarce Chondrites burrows, even if the overall bioturbation intensity is very low.The combination of trace-fossil assemblage and lithofacies of the Oued Fodda Formation indicates relatively stable outer shelf environments below the storm wave base, which corresponds classically to the lower offshore to shelf edge environments, and the prevailing palaeoecological conditions are optimal and stressful for the benthic organisms.

Keywords Zoophycos, Ethology, Palaeoecology, Lower Cretaceous, Ouarsenis Mountains, Algeria

1.Introduction

Zoophycos Massalongo, 1855 is one of the most enigmatic trace fossils in the sedimentary records since its first descriptions in the 19thcentury,in regard to its high morphological variations and various environmental distribution which are controlled by several palaeoecological parameters such as substrate consistency, sedimentation rate, and palaeobathymetry(Bottjer et al., 1988; Olivero, 1996, 2003; Kotake,2014; Richiano, 2015; Zhang et al., 2015a).However,after almost two centuries of studies, the morphology of Zoophycos and the ethology of its producers still remain unsolved and debated intensely, especially in the last decades, which resulted in several constructional models (e.g., Bromley and Hanken, 2003;Olivero, 2003; Olivero and Gaillard, 2007; Seilacher,2007; Monaco et al., 2017; Belghouthi et al., 2020)and ethological interpretations (e.g., Wetzel and Werner, 1981; Kotake, 1989, 1992; Fu and Werner,1995; Olivero and Gaillard, 1996; L¨owemark and Sch¨afer, 2003; Gong et al., 2008; Knaust, 2009a,2009b;L¨owemark,2012,2015;Bayet-Goll et al.,2020).The trace makers are inferred to be various worm-like animals such as echiurids (Kotake, 1992), polychaetes(Ekdale and Lewis, 1991; Knaust, 2009a; Zhang and Zhao, 2016), and sipunculids (Wetzel and Werner,1981; Olivero, 2003; Olivero and Gaillard, 2007).Thus, the ichnotaxonomic status of Zoophycos is still a matter of debate among researchers due to the extreme complexity and high morphological variability of the traces(e.g.,Olivero,2007);therefore,they are mostly ascribed to the ‘Zoophycos group’ (Uchman,1995), which is believed to be more operational by the researcher than the determination of the ichnospecies.However, the ichnospecies approach has not yet disappeared and has recently been strongly recommended by some authors (Mekki et al., 2019; Vinn et al.,2020;Bouchemla et al.,2021a,2021b,2023).

Zoophycos ichnofacies is named after the homonymous ichnogenus and is generally developed in muddy deposits with oxygen deficiency and rich in organic matter from the outer shelf to bathyal zones, dominated by complex fodinichnial burrows with a low ichnodiversity (Seilacher, 1967, 2007; Frey and Pemberton, 1985; Buatois et al., 2002; MacEachern et al., 2007a, 2007b; Buatois and M′angano, 2011;Richiano, 2015; Bouchemla et al., 2023).However,throughout the Phanerozoic, Zoophycos occurs in a high variety of depositional settings, from stormdominated shallow-marine environments in the Paleozoic (e.g., Gaillard et al., 1999; Knaust, 2009a;Zhang, 2014; Zhang and Zhao, 2015; Zhang et al.,2015b; Li et al., 2017; Sedorko et al., 2018; Abasaghi et al., 2020; Bouchemla et al., 2021a), to outer shelf and deep-sea sediments in the Mesozoic and Cenozoic(e.g., Wetzel and Werner, 1981; Olivero, 1996, 2003;Wetzel et al., 2007; L′opez-Cabrera et al., 2008;Kotake, 2014; Richiano, 2015; Monaco et al., 2017;Mekki et al.,2019;Belghouthi et al.,2020;Vinn et al.,2020; Bouchemla et al., 2023), with some rare exemptions (e.g., Giannetti et al., 2017).During the Cretaceous,Zoophycos was characterized by large and complex burrows with lobed spreiten,found generally in the outer shelf to deep-sea deposits with oxygendeficient interstitial waters (Olivero, 2003; Seilacher,2007; Zhang et al., 2015b).This is reflected by the evolutionary trend of Zoophycos from the Early Jurassic to the Late Cretaceous in the French Subalpine Basin (Olivero, 2003), where the most complex and numerous morphotypes are restricted to deeper environments from the Early Cretaceous onward.

In the A?n Hadjela area (Ouarsenis Mountains) in northwestern Algeria, Zoophycos occurs locally with abundance in the Lower Cretaceous Oued Fodda Formation,composed mainly of limestones and marls.The study aims to analyze the ethology and morphological characteristics of abundant Zoophycos in the Lower Cretaceous succession from Algeria and to discuss the palaeoecological factors controlling their occurrence patterns according to the palaeoenvironmental context of the deposits studied.

2.Geological setting

The Ouarsenis area is characterized by a mountain range that stretches for nearly 200 km.It occupies the southern edge of the Tellian domain in northwestern Algeria,bounded by the Ch′elif plain to the north and the High Plateaus to the south (Fig.1A).The Kef Sidi Amar zone(=High Peak zone)(Fig.1B),is the highest mountainous peak in the Ouarsenis area and even in western Algeria.Due to its high and central location within the Ouarsenis,it's now considered as the major zone to subdivide the Ouarsenis Mountains into an eastern and a western Ouarsenis Mountains area.On the other hand, the lithostratigraphic succession of the Ouarsenis culminating zone has been elaborated on by several decades of studies, and several formations have been proposed (Mattauer, 1958; Polv^eche,1960; Tchoumatchenco, 1986; Tchoumatchenco and Khrischev, 1992; Tchoumatchenco et al., 1995;Benhamou,1996;Benyoucef, 2006).Structurally,the Ouarsenis Mountains have extremely complicated tectonic characteristics (e.g., tectonic deformation,fault-propagation folding, thrust or reverse faults).Like the vast majority of the Tellian domain, it is marked by autochthonous and allochthonous units(nappes), which originated because of the “paroxysmal phase” of the intra-Miocene movement(Mattauer,1958;Polv^eche,1960;Wildi,1983).In this way,the Djebel El Bayadha outcrops(studied section)correspond to the allochthonous unit, whereas the outcrops in Ouarsenis culminating zone are considered overturned outcrops,corresponding to the paraautochthonous unit.

Palaeogeographically, the Early Cretaceous of the study area coincided with the opening period of the Tethys Sea(Fig.1C).This domain has been characterized by the presence of scattered microplates in the middle of the Tethyan oceanic corridor between the European and African continents(Cecca,1998).In the study area,the Berriasian－Valanginian is marked by a transgressive episode analogous to the Tethys palaeo-provinces(e.g.,Spain;Company,1987)and represented by hemipelagic and pelagic deposits(Cherif et al.,2021).

Fig.1 Location of the study area and the studied section.A) Geographical position of the study area in relation to the major geographical features of northwestern Africa;B)Location map of the studied section at 3 km southwest of the village of Bouca?d,the northwestern part of the Ouarsenis culminating zone.Dj.= Djebel; C) Palaeogeographic reconstruction of the Early Cretaceous (Berriasian－Valanginian) (after Scotese, 2014).

Strata of the Ouarsenis Mountains are characterized by a complete sedimentary succession ranging from Triassic to Quaternary, with a Paleozoic basement of porphyritic rocks (Glangeaud, 1951; Calembert, 1952;Mattauer, 1958), sometimes included in the Triassic strata.The Triassic is represented by multi-coloured clays, gypsum, and cargneules (carbonate rock with a carious and vacuolar aspect) intercalated by scarce dolostones and limestones (Mattauer, 1958; A?fa and Zaagane, 2014).The Jurassic outcrops are dominated by carbonate formations, intercalated infrequently with sandstone layers.The Lower Jurassic mainly contains dolomite facies, with dolomitic limestones and oolitic compact limestones upward (A?fa and Zaagane,2014).The change in the carbonated characters is distinct during the Toarcian,marked by the appearance of alternating marl and limestone, containing brachiopod fauna (e.g., Quadratirhynchia attenuata)(Almeras and Elmi, 1982).The Upper Jurassic of the Ouarsenis Mountains is generally represented by pelagic carbonate platform deposition.This is due to extensive tectonic movements during the Late Jurassic that led to deeper-water sedimentation, mainly dominated by deposits of the“Ammonitico Rosso”facies(Sadji et al.,2021).

The Cretaceous of the Ouarsenis Mountains is characterized by the deposition of a moderately thick carbonate deposit in the lower part, often constituting of marl－limestone alternation (Oued Fodda Formation),and inheriting the continuity of the Jurassic sedimentation, without marked transition due to lithologic continuity (Benyoucef et al., 2022).The carbonate facies disappeared with the onset of a thick formation of 1500 m,constituted essentially by sandy-argillaceous alternation (El Malaab Formation) rich in trace fossils,sedimentary structures,slumps,olistoliths,and Bouma sequence members, giving evidence of turbidite deposition (Kireche, 1993; Tchoumatchenco et al., 1995;Benyoucef, 2006).The return to carbonate facies is heralded in its totality by the deposition of greyish marls with scarce limestone beds in the Upper Cretaceous, represented by several formations (i.e., Rhedadoua,Hassin Ben Ziane Djilali,and Ouled Djilali).

There are no visible unconformities from the Upper Cretaceous to the Cenozoic.However, during the Paleogene, the deposits of the Ouarsenis Mountains usually contained marls, except for the period between the Paleocene and the Early Eocene, which is characterized by marly and sometimes sandyglauconitic limestone facies (Mattauer, 1958).In the eastern part of the Ouarsenis Mountains,the Oligocene is generally represented by thick sandstone deposits overlying on argillaceous series denoting the Numidian facies(Wildi,1983).The Lower and Upper Miocene are inseparable, represented by marly deposits that evolve upward to another sedimentation regime dominated by sandstone deposits.The latter progresses laterally towards the west in often conglomeratic reddish formations (Mattauer, 1958).Gravel veneers and carbonated crust mark the Plio-Quaternary.

3.Material and methods

The Lower Cretaceous Oued Fodda Formation represents marl－limestone alternations that crop out in the A?n Hadjela area (GPS: 35°52′52.01′′N;01°35′44.11′′E; Fig.1B).The ichnological content is represented by abundant Zoophycos specimens mainly observed within the mud-to-wackestone texture,associated with poorly diversified trace-fossil assemblage, which have been collected and photographed under natural light in situ during the fieldwork.However,the description and morphometric measurements of the trace fossils(e.g.,branching,lining,and width of Zoophycos spreiten) were directly carried out in the field or later in the laboratory by using field photographs.Sedimentological features, including primary sedimentary structures, bedding contacts, bed thickness, textures, and skeletal and non-skeletal components, were also considered and photographed in the field.A total of 63 samples were collected along the lateral extent of the Oued Fodda Formation, among them 19 samples for petrographic studies to improve field description and lithofacies based on its microfacies characteristics (fossil content, grain size, grain composition, and sedimentary texture) using the carbonate rock classification of Dunham(1962)and Embry and Klovan(1971).To assess the bioturbation intensity,we used the bioturbation index (BI) according to the criteria of Taylor and Goldring (1993), and to estimate the density of Zoophycos,we followed Olivero's(1994)scaling.Furthermore, the ichnospecies assignments of the Zoophycos specimens of the Oued Fodda Formation are based on the systematic revision and ichnotaxonomy of Zoophycos conducted by Zhang and Gong(2012).Therefore, the ichnogenus Zoophycos is revised into nine ichnospecies, including Zoophycos cauda-galli Vanuxem (1842) and Zoophycos brianteus Massalongo(1855), which are the main ichnospecies recorded within the studied formation.The authors consider that the morphological characteristics (overall shapes), dimensions of the spreite, and outline are the main features used for identification and differentiation at the ichnospecies level.

4.Lithological and sedimentological characteristics of the Lower Cretaceous Oued Fodda Formation

The biostratigraphic assignment of the Oued Fodda Formation is based on the biozonation established by Tchoumatchenco et al.(1995) and more recently by Cherif et al.(2021), showing its deposition between Berriasian and Valanginian times.Benyoucef et al.(2022) characterized in detail interesting crinoid assemblages.Trace fossils were also studied in details by Cherif et al.(2021).

The study area is located approximately 3 km southwest of the Bouca?d mining village and 5 km north of the town of Bordj Bouna^ama(Fig.1B),which occupies the large depression of the A?n Hadjela.The outcrops studied are located on the southern flank of Djebel El Bayadha,1.5 km west of the national road Rn19(Fig.1A and B).The Oued Fodda Formation (Tchoumatchenco et al., 1995) conformably overlying the A?n El Hamra Formation, which is dominated by the “Ammonitico Rosso” facies of Oxfordian－Berriasian age (Figs.2 and 3A).Above and in unconformable contact is the detrital-dominated El Malaab Formation of Barremian－Albian age (Tchoumatchenco et al., 1995;Benyoucef,2006).Basedonits lithological,ichnological,and stratonomical characteristics,the Oued Fodda Formation is subdivided into four informal units (Unit 1－Unit 4 from the bottom to the top;Fig.2).

4.1.Lithological descriptions

4.1.1.Unit 1: Marl－massive to nodular limestone alternation (38 m)

This unit consists of an alternation of reddish to greenish marls (0.20 m－1.10 m) with massive to nodular limestone beds (0.05 m－0.70 m) containing intraclasts of different sizes (Fig.3B).The beds are laterally continuous, bluish to greenish in colour, and rich in ammonites and belemnites.The top surface is marked by asymmetric ripple marks and bioturbation filled with greyish to yellowish material(Fig.3C).The interbedded marls (0.20 m－1.10 m thick) yield calpionellids, pelagic crinoids, ophiuroids, planktonic foraminifers, and aptychi.Microscopic analysis shows biomicrite of wackestone－packstone texture rich at the base of the unit in ossicles of roveacrinids and Saccocoma (Fig.4A－C), and thin-shelled bivalves(Posidonomya sp.) (Fig.4D), associated with calpionellids, planktonic foraminifers and ammonites, and rare saccocomids at the top (Fig.4E and F).

4.1.2.Unit 2: Bioturbated limestone－marl alternation (45 m)

This unit begins with a deep bioturbated bluish limestone bed (0.40 m), which confers a brecciated appearance.This unit is topped by an alternation of beige to greenish marl(0.20 m－1 m) with centimetric limestone beds(0.10 m－0.30 m),sometimes with soft,grey argillaceous limestones,and occasionally greenish to bluish limestone plaques.The contact between these beds is clear, sometimes slightly undulating.The limestone beds are characterized by a wealth of pelagic fauna encompassing abundant ammonites and belemnites, as well as bioturbation mostly represented by

Thalassinoides,Chondrites,and Zoophycos.Microfacies characteristics reveal mudstone－wackestone-textured biomicrite with calpionellid sections, Saccocoma, and thin-shelled bivalves(Fig.5A－C).The marls reveal the presence of smooth-shelled ostracods, roveacrinid ossicles,and benthic and planktonic foraminifers.

4.1.3.Unit 3: Marl－laminated limestone alternation (18 m)

This unit is composed of an alternation of gray to blueish marls (0.10 m－0.80 m) and greyish laminated limestone beds (0.10 m－0.25 m) rich in pyritic ammonites and belemnites(Fig.3D and E)with rare bivalve shells and gastropods.Some limestone beds are characterized by the presence of trace fossils assigned to Chondrites and Zoophycos.The marl deposits show both planktonic and benthonic foraminifers, and crinoids.Microfacies analysis documents a predominance of biomicrite mudstone-textured limestone,including mostly skeletal components represented by radiolarians, siliceous sponges,and rare roveacrinid sections(Fig.5D).

4.1.4.Unit 4: Marl－massive limestone alternation(6 m)

This last unit is not complete due to the denudation peak.Existing outcrops show alternating greenish marls(0.30 m－0.45 m)and blueish-to-greyish massive limestone beds (0.30 m－0.80 m) with a slumped appearance.The marly interbeds contain both planktonic and benthonic foraminifers and pelagic crinoids.The texture is dominated by biomicrite mudstone with radiolarian sections (Fig.5E and F).

4.2.Depositional environments

Fig.2 Lithostratigraphic column of the Oued Fodda Formation showing the distribution of the recorded trace fossils, textural evolution,Zoophycos density class number, depositional environments with water depth change, and palaeooxygenation.Note that the palaeooxygenation curve is built approximatively according to the ichnological data.

Fig.3 Field photographs of the Oued Fodda Formation.A)Panoramic view of the Djebel El Bayadha section(A?n Hadjela area),showing the contact between the A?n El Hamra Formation and the Oued Fodda Formation;B)Panoramic view showing an alternation of reddish to greenish marls and massive limestone beds (Unit 1); C) Top surface of limestone bed (Unit 1) showing moderately to strongly bioturbation by Thalassinoides burrows (see white arrow) and including ammonite fauna (see black arrow); D－E) General appearance of the greyish laminated limestone beds (Unit 3).Note the presence of pyritised belemnite rostra (see black arrows) and ammonites (see white arrow).

The Oued Fodda Formation corresponds to pelagic sedimentation of an open marine platform, which is marked by the development of carbonate deposits that shows textural evolution through the succession,ranging from packestone(Unit 1)to mudstone(Unit 4).However, the evolution of the depositional environments and water depth curve are shown in Fig.2, in which the dominant ramp depositional environment corresponds to different lithologies.

Fig.4 Photomicrographs of thin sections from the Oued Fodda Formation outcropping in the Djebel El Bayadha section(A?n Hadjela area).A－D) Microfacies characteristics from the base of Unit 1 show a wackestone－packestone texture with roveacrinid ossicles (A－C; see blue arrows)and thin-shelled bivalves(Posidonomya sp.)(D);E－F)Microfacies characteristics from the top of Unit 1 show biomicrite wackestone with roveacrinids (E, black arrows), calpionella sections (F, white arrow), and planktonic foraminifers (F, red arrow).

The lower part of Unit 1 is mainly formed by an irregular alternation of marl and limestone beds, as well as carbonate nodules.It contains some pelagic fauna (ammonites and belemnites) with rare Thalassinoides burrows.Asymmetrical ripple marks occurred in some limestone layers,containing intraclasts,and thus offering a packestone texture, rich in ossicles of roveacrinids and thin-shelled bivalves (Posydonomia sp.).In opposition,the upper part of this unit reveals a more variable texture ranging from wackestone to packestone rich in Calpionella sections and planktonic foraminifers, showing an upward-deepening trend.However, the dominance of wackestone－packstone texture reflects moderate wave energy (Aigner, 1982),but slightly under the influence of storm waves.These textural results are possibly closely related to storm events below the fair-weather wave base.Moreover,intraclasts indicate bottom currents that erode an unlithified substrate.To this end, the presence of asymmetrical ripples and dwelling－feeding burrows(Thalassinoides) at the top of some limestone beds reflect a low rate of fair-weather sedimentation(e.g.,Fürsich et al.,2018;Cherif et al.,2021),and document therefore, offshore conditions probably the upper offshore zone for this part of the formation(Unit 1).

Fig.5 Photomicrographs of thin sections from the Oued Fodda Formation outcropping in the Djebel El Bayadha section(A?n Hadjela area).A－C) Microfacies characteristics from the bioturbated limestone－marl alternation (Unit 2) show a mudstone－wackestone-textured biomicrite including some thin-shelled bivalves (Posidonomya sp.) (see blue arrows) in association with a rich concentration of calpionella sections; D) Mudstone-textured biomicrite from the marl－laminated limestone alternation (Unit 3) showing a roveacrinid section (see the black arrow); E－F) Mudstone-textured biomicrite from the massive limestone beds (Unit 4) with radiolarian sections (see red arrows).

Unit 2 is formed by an alternation of marl and limestone layers, mainly bioturbated, showing a biomicritic mudstone－wackestone texture rich in calpionellid sections, roveacrinids, and thin-shelled bivalves.It is characterized by a wealth of pelagic fauna encompassing abundant ammonites and belemnites.

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Similarly, Unit 3 is characterized by laminated,greyish to dark greyish,purely micritic carbonate rocks rich in pyritic pelagic fauna (ammonites).Its microfacial analysis showed a biomicritic mudstone texture that contained sections of radiolarians and roveacrinids.The fine-grained sediments, interpreted as suspension deposits, and the abundance of macrofauna of the open marine environment (ammonites)and accompanying microfauna such as thin-shelled bivalves, calcispheres, and pelagic crinoids of the Oued Fodda Formation indicate a low-energy, deep outer shelf/ramp environment (Unit 2) shifting to lower offshore to continental shelf margin (Unit 3)setting (e.g., Lukeneder et al., 2012), which issupported by the lack of neritic benthic macrofauna and the absence of sedimentary structures (e.g.,hummocky cross-stratification) and coarse-grained textures indicative of strong bottom currents.These sedimentary features indicate that the settling of finegrained suspended material is practically the only sedimentary process operating in an environment where calm hydrodynamic conditions dominate.However,the marl－laminated limestone beds(Fig.3D and E) characterizing Unit 3 indicate a short duration of low bottom current (Cherif et al., 2021).The palaeoenvironment interpretation (i.e., deep outer shelf/ramp) is also supported by the presence of some crinoid groups (Isocrinida, Cyrtocrinida, and Roveacrinida)typical for distal depositional settings located below the storm wave base (Benyoucef et al., 2022).An outer shelf (outer ramp) environment was also proposed by Cherif et al.(2021) and Benyoucef et al.(2022) for these units of the Oued Fodda Formation.

Size－－Small to medium Small to medium Largest Largest Shallow to medium Depth Medium Upper SWB between SWB and FWWB(inner ramp) Shallow－－Deepening Lower SWB(outer ramp)Depositional environment Absent－－Lower SWB Rare(about 2 traces/10 m2)Lower SWB(just below SWB)Density Very rare(1 trace/10 m2)Common (at least 1 trace/2 m2)Abundant (at least 1 trace/m2;Zoophycos occasionally touching each other)Very abundant(the bed surface is totally covered by Zoophycos)Zoophycos Class 0 Class 1 Class 2 Class 3 Class 4 Class 5

The latest unit(Unit 4)is characterized by slumped radiolarian-bearing fine-grained limestone beds lacking sedimentary structures which indicate violent bottom currents, suggesting a continental shelf edge(beginning of the continental slope?).The absence of redeposited carbonate sediments by mass－flow processes and turbidite-like flows supports such interpretation.These sedimentary features may indicate the deepest depositional condition during the deposition of the Oued Fodda Formation, and therefore an overall increase in the water depth towards the top of the studied section.

5.Zoophycos ichnofacies in the Oued Fodda Formation

The Oued Fodda Formation of the studied section shows an ichnological assemblage that is typical of the Zoophycos ichnofacies (Buatois and M′angano, 2011;MacEachern et al., 2012), with six ichnotaxa (i.e.,Zoophycos brianteus, Zoophycos cauda-galli, Chondrites intricatus, Ophiomorpha isp., Planolites isp.,and Thalassinoides isp.)observed only in Units 2 and 3(see Fig.2).This ichnofacies is widely distributed in open and deep marine environments below the storm wave base(e.g.,Mekki et al.,2019;Vinn et al.,2020;Bouchemla et al.,2021a,2023),and is often linked to stressful palaeoecological conditions such as oxygen deficiency.The distribution of Zoophycos within the Oued Fodda Formation is mainly restricted to the two middle units(bioturbated limestone－marl alternation and marl－laminated limestone alternation).The ichnodiversity is very low which shows,in addition to the Zoophycos,the existence of other trace fossils such as Chondrites, Ophiomorpha, Planolites, and Thalassinoides.The bioturbation intensity is generally low(BI=0－1)in the large part of the formation except for Units 2 and 3, where they preserved almost all trace fossils revealing a variable degree of bioturbation(BI =3－4)in several layers.

5.1.Descriptions of Zoophycos through the section

5.1.1.Zoophycos brianteus Massalongo, 1855

The observed Zoophycos specimens in the upper part of Unit 2 are generally characterized by a medium to high density(class 3 to 4 sensu Olivero,1994)(Table 1), showing a high degree of bioturbation intensity reaching grade 4.They are represented by large,flat,spiral-shaped spreiten with variable diameters between 45 cm and 75 cm (Fig.6A－C).The spreite is horizontal, developed parallel to the stratification with a dextral and/or sinistral coiling.The marginal tube is rarely preserved and the infill of the lamellae is similar, sometimes slightly different from that of the host rock.The outline of the trace is irregular as a result of the diversion of the marginal tube every so often because of the presence of the body fossils(e.g.,ammonite in Fig.6A and B).Primary lamellae are evenly spaced (2 mm－4 mm) starting from a central point(burrow apex),and bending slightly towards the distal parts of the spreiten.These forms are assigned to Zoophycos brianteus Massalongo(1855)(Fig.6A－C),the type ichnospecies of Zoophycos(Olivero, 2007).

Fig.6 Zoophycos from the Oued Fodda Formation outcropping in the Djebel El Bayadha section (A?n Hadjela area).A) and C) Large and flattened,spiralling-shaped spreitens assigned to Zoophycos brianteus,showing dextral and sinistral coiling;B)Partial enlargement of Fig.6A for details showing the deviation of the external outline by the Zoophycos-producer organism during the feeding process in response to an obstacle in the sediment (e.g., ammonite fossil; see white arrow).Abbreviations: ap = apex; la = lamellae; mt = marginal tube.

5.1.2.Zoophycos cauda-galli Vanuxem, 1842

Fig.7 Zoophycos from the Oued Fodda Formation outcropping in the Djebel El Bayadha section (A?n Hadjela area).A－B) U-shaped specimens, assigned to Zoophycos cauda-galli reported from the upper part of Unit 2; C－D) Small coiled Zoophycos brianteus reported from the upper part of Unit 2; E－F) Cross-sectional views of Zoophycos spreiten (Zo) show the alternation of dark and light menisci in the internal backfill structure.Note that the direction of concavity corresponds to the direction of lateral shifting of the marginal tube.Abbreviations:ap = apex; la = lamellae; mt = marginal tube.

To the top of the unit (Unit 2), considerable Ushaped specimens assigned to Zoophycos cauda-galli Vanuxem (1842) (Fig.7A and B) appeared with low density (class 2, rare).The specimens are preserved as U-shaped full relief burrows, 20 cm－25 cm long,with an average width of 15 cm.Primary lamellae are well developed, 2 mm－3 mm apart, which are most often surrounded by a marginal tube of 3 mm in diameter, and are completely devoid of secondary lamellae.Additionally, a small number of coiled Zoophycos specimens assigned to Zoophycos brianteus are present.These forms are characterized by an upward spirally coiled lamina showing wellpreserved and clearly primary lamellae without secondary lamellae(Fig.7C and D).The length of the structure is difficult to estimate due to the weathering, but is estimated to be up to 12 cm.In crosssectional view, Zoophycos appear as a continuous ribbon formed by the succession of several parabolic meniscus structures of variable length (several tens of centimetres) and almost constant width of 4 mm－5 mm (Fig.7E and F).Zoophycos-bearing levels exhibit a less intense degree of bioturbation (between 1 and 2) in contrast to the Zoophycos-rich bed from the middle part of Unit 2.

The marl－laminated limestone alternation(Unit 3)displays scarce trace fossils,generally represented by relatively smaller Zoophycos than the large,flattened coiled specimens from the middle part of the previous unit(Fig.8A and B).They consist of plane,spiralling,Jshaped spreiten surrounded by a small marginal tube(3 mm－5 mm in diameter),with an overall diameter of 25 cm－35 cm, showing both sinistral and dextral construction of the lamina.Zoophycos are preserved as full relief in a purely micritic facies of mudstone texture.Chondrites intricatus is sparser,with a similar morphology to the previous unit, associated with Ophiomorpha isp.

5.2.Associated trace fossils

Chondrites intricatus Brongniart (1828) (Fig.9A and B)

The upper part of Unit 2,is marked by the presence of abundant Chondrites (often co-occurring with Thalassinoides isp.),as represented by small,straight,short,tree-like branching burrow systems,assigned to the ichnospecies.The Chondrites trace fossils are preserved in full relief and have different fillings from the host rock, which allows the distinction of two varieties: the first variety consists of first-order branch burrows with acute angles(30°－45°),0.5 mm－0.8 mm in diameter and 2 mm－5 mm long, with dark micritic filling and displays smaller second-order branches(Fig.9A); the burrows of the second variety are in association with tiny burrows of Thalassinoides,0.5 mm in diameter and 5 mm－10 mm long (Fig.9B), and are characterized by lighter filling,irregular branches of a 45°angle,and the absence of second-order branches.Chondrites are common in a wide range of lithologies and environments, with a number of behavioural models.It is interpreted commonly as fodinichnion,chemichnion, and agrichnion burrows produced by diverse trace makers (e.g., annelids, sipunculoids, or even chemosymbiotic bivalves; Baucon et al., 2020).

5.2.2.Ichnogenus Ophiomorpha Lundgren, 1891

Ophiomorpha isp.(Fig.9C and D)

It corresponds to horizontal, branched, straight to inclined Y-shaped burrows, preserved in full relief exclusively in Unit 3.The filling is identical to the host rock, whereas the burrow wall is covered by ochrecoloured (pyritised) low subconical granules regarded as pellets.Measures are about 1.5 cm－2 cm in diameter and have a variable length, sometimes up to 30 cm(Fig.9C).The bioturbation intensity of this unit is generally low (BI = 0－1).Ophiomorpha is interpreted as a domichnion structure,produced commonly by thalassinoid shrimps (Patel and Desai, 2009;Bouchemla et al., 2020; Bendella et al., 2021; Mekki et al., 2023).

Fig.9 Trace fossils from the Oued Fodda Formation outcropping in the Djebel El Bayadha section(A?n Hadjela area).A)Chondrites intricatus filled with dark micritic material different from the host rock;B)Chondrites intricatus(Ci)and small Thalassinoides isp.(Th);Note that both trace fossils are filled with lighter material than the host rock and that Thalassinoides isp.cross-cutting Chondrites intricatus; C－D)Ophiomorpha isp.preserved in full relief exclusively in Unit 3;E)Highly bioturbated limestone bed by dark Planolites isp.burrows recorded in the upper part of Unit 2.

5.2.3.Ichnogenus Planolites Nicholson, 1873

Planolites isp.(Fig.9E)

Planolites isp.are represented as endichnial, full relief, simple, unlined, unbranched, subcylindrical,flattened,straight to curved burrows,with 3 mm－4 mm in diameter and a few centimetres long,and preserved only within Unit 2.The burrows are actively filled with sediments of different colour(grey to black)compared with the host rock, and are cross-cutting themselves,showing a high degree of bioturbation(BI=4).Planolites is interpreted as a deposit-feeding trace,probably produced by diverse,mainly worm-like organisms(Uchman,1995;Bouchemla et al.,2020;Mekki et al.,2023).

5.2.4.Ichnogenus Thalassinoides Ehrenberg, 1944

Thalassinoides isp.(Fig.9B)

It corresponds to horizontal, smooth, elliptical,flattened tunnels with Y-shaped branches.The diameter is variable (5 mm－8 mm) and the length is from 20 mm to 30 mm,having the same filling as the second variety of Chondrites.This association is preserved in full relief in biomicrite wackestone－mudstonetextured limestones.However, the overall bioturbation is moderate,occasionally reaching 4(BI=4);sometimes Thalassinoides cross-cutting Chondrites show a shallow tiering.Thalassinoides are a faciescrossing ichnotaxon, generally interpreted as domichnial and/or fodinichnial burrows produced by crustaceans (Knaust, 2017; Bouchemla et al., 2020,2021a;Bendella et al., 2022; Mekki et al., 2023).

6.Discussion

6.1.Ethological analysis of Zoophycos and trace maker

The behaviour of Zoophycos has been discussed for a long time,resulting from different ethological modes for the trace maker (see L¨owemark, 2015, and references therein).However,different strategic behaviour of the producer could be observed in the same specimen of Zoophycos(Knaust,2009a).In the Oued Fodda Formation of the studied section, Zoophycos are recognized as large J-shaped and U-shaped with distinctive lamellae and marginal tubes with the same material as the host rock.The similarity of the fillings in the burrows and the surrounding sediments indicates that the producer has only used the available materials in the sediment for feeding (e.g., Abasaghi et al., 2020).Moreover, the long and curved nature of J-shaped or U-shaped protrusive burrows without evidence of consolidation in the spreiten implies that their producer is a deposit feeder (Bayet-Goll et al.,2020).The occurrence of Zoophycos only in Units 2 and 3 and specifically in some muddy limestone beds suggests that the producer chose a substrate with high organic matter.The large and flattened, shallowtiered spiral J-shaped protrusive burrows recorded within Unit 2, cover a large surface in the substrate(30 cm－75 cm in diameter), which indicates the availability of nutrient food good enough for growth under good palaeoecological conditions, far from competition from other benthonic fauna.According to Gaillard and Olivero (1993), the lateral and vertical arrangement of the spreiten depends on the concentration of organic matter and oxygen level.Consequently, the producer's behavioural strategy in the nutrient-rich substrate is of the deposit-feeding type(e.g.,Olivero and Gaillard,2007;Knaust,2009a;Zhang et al., 2015a).In such a situation, the producer, by developing horizontal to slightly inclined U-shaped or J-shaped protrusive burrows, makes it easy to get access to the nutrients without needing deep tiering.Additionally, non-faecal pellets are observed within the Zoophycos spreite of the Oued Fodda Formation,which indicates that the producer did not defecate in the sediment or move to the water－sediment interface at the time of defecation(Knaust,2009a,2009b;Zhang and Zhao, 2016; Bouchemla et al., 2023);therefore, the pelleting behaviour for the producer is excluded.All these features indicate that the producers represent a deposit-feeding model.

Although the origin of the Zoophycos producer has not yet been found in its burrow, several hypotheses have been proposed in recent decades with several candidates therefore being assumed.It is most commonly referred to a small as worm-like organism such as sipunculans(Wetzel and Werner,1981;Olivero,2003;Knaust,2004).However,the complex morphology and the evolutionary trend of the palaeoenvironment through the Phanerozoic suggest that the producer should be a long-ranging conservative taxonomic group or Zoophycos may be the product of several taxa with similar lifestyles(Zhang et al.,2015a).Zoophycos from the Oued Fodda Formation morphologically resembles the Early－Late Cretaceous French Zoophycos(Olivero,2003).The marginal tube of the described specimens through the section is slightly long but of a small diameter.This suggests a marine-feeding animal living in muddy sediments (Olivero, 2003).It seems, therefore, that the worm-like animal represented by sipunculans is the producer of the Zoophycos in the Oued Fodda Formation, as has been proposed for the Cretaceous French Zoophycos(see Olivero,2003).

6.2.Palaeoecological factors controlling Zoophycos

Zoophycos are the most important and abundant burrows of the carbonate platform sequences of the Oued Fodda Formation,formed in a fully marine outer shelf setting(lower offshore zone to continental shelf edge).However,the sedimentation rate,benthic food supply, and amount of oxygen are the most important palaeoecological features controlling the development of Zoophycos ichnofacies in the Oued Fodda Formation (Units 2 and 3).

6.2.1.Sedimentation rate and benthic food supply

It is evident that the sedimentation rate plays an important role in the distribution of Zoophycos(Savrda and Bottjer, 1989; Gaillard and Olivero, 1993; Olivero and Gaillard, 1996; Kotake, 2014; Richiano, 2015;Nasiri et al., 2018; Bouchemla et al., 2021a, 2021b).Furthermore, a low sedimentation rate is a necessary factor to ensure the best conditions for burrow construction (e.g., Olivero, 1994; Nasiri et al., 2018;Bouchemla et al.,2023).Low sedimentation rates could have allowed the accumulation of huge amounts of benthic food in quiet settings, usually from the outer ramp zone onward.In this regard, the increased bioturbation in the deposits by the animals producing trace fossils, Zoophycos among them.The large specimens assigned to Zoophycos brianteus observed predominantly in Unit 2 were developed in a lower offshore environment below the storm wave base.This is considered as a stable environment, which promotes the accumulation of large amounts of benthic food,supported by the low sedimentation rate.These conditions are perfect for Zoophycos trace makers to explore large volumes of high-nutrient sediment to form shallow-tier, large- to medium-sized J-shaped coiled burrows.In contrast, Paleozoic Zoophycos are mainly related to the high sedimentation rate brought by storm-generated currents, which prevents the accumulation of organic matter in seafloor deposits;therefore, Zoophycos producers mainly formed short and a few medium lobes with small diameters (e.g.,Zhang,2014;Li et al.,2017;Bouchemla et al.,2021a).However,despite the environmental situation of Unit 2(i.e.,the lower offshore zone),the specimens observed in the top unit are small-coiled with abundant U-shaped morphotypes (Zoophycos cauda-galli).They were constructed approximately in a deeper and quieter water environment, rather than for the large Zoophycos brianteus recorded in the middle unit.Although the deposits laid in a low-energy environment with low sedimentation rates, the Zoophycos-organism formed medium- to short-lived Zoophycos.This seems to be related to stressful conditions rather than sedimentation rates occurring at the summit of the unit, which prevents Zoophycos organisms from building large burrows in the muddy limestone beds.In summary, the development of Zoophycos in the Oued Fodda Formation appears to be related to the availability of benthic food, which is controlled by the dilution effect caused by the sedimentation rates.

6.2.2.Oxygenation

Oxygenation within sediments is an effective factor in controlling the living conditions of mudfeeding organisms such as Zoophycos trace makers,which also influences the amount of penetration within seafloor deposits (Nasiri et al., 2018;Bouchemla et al.,2021a).In the section studied, the diameters of Zoophycos are large with coiled J-shaped to slightly small coiled U-shaped morphotypes.The large size of J-shaped Zoophycos recorded in the middle part of Unit 2, might imply that the Zoophycos-producing organisms exploited nutrient-rich sediments under well-oxygenated and stable conditions (e.g., Vinn et al., 2020; Bouchemla et al.,2021a).Furthermore, J-shaped burrows would be sufficient under conditions of a normal oxygenation environment (Wetzel and Werner, 1981; Wetzel,1991; Bromley and Hanken, 2003).Consequently,the oxygen level during the deposition of the middle part of Unit 2 is significantly high, which allows Zoophycos-producing organisms to take the opportunity to explore large surfaces of the seafloor deposits rich in benthic food.However, the upper part of the unit reflects inhospitable conditions (anoxia in bottom waters;cf.Cherif et al.,2021), explained by shallow tier levels of Chondrites and tiny specimens of Thalassinoides,as well as trace fossils of Planolites.This low diversity assemblage is co-occurring mostly with U-shaped and small-coiled Zoophycos burrows, with their shallow penetration implying dysoxic conditions(Richiano, 2015) for the Zoophycos ichnofacies.According to Wetzel and Werner(1981),the open U-tube allowed the circulation of seawater under lowoxygenated benthonic conditions, which explains the occurrence of these specimens in contrast to other morphotypes under such conditions.Furthermore, the appearance of well-laminated limestone beds textured with grey to dark mud to wackestone in the upper part of Unit 2 and the lower part of Unit 3 with the scarcity of benthonic faunal elements and the abundance of pyritic pelagic fauna, thus characterizing low-resource, oxygen-depleted environments(Bromley,1990;Richiano,2015;Uchman et al.,2016), and the scarcity to paucity of bioturbation within sediments confirmed this interpretation.However, toward the top of Unit 3, clearly J-shaped spiral spreiten without lobe spreiten, assigned to Zoophycos brianteus, appeared in a greyish mudstone-textured limestone bed, in association with Ophiomorpha ichnogenus and very scarce Chondrites, showing that the oxygenation of the seafloor improved considerably.

7.Conclusions

The Lower Cretaceous (Berriasian－Valanginian)Oued Fodda Formation in the Ouarsenis Mountains is characterized by a carbonate sedimentation succession rich in pelagic fauna.It is subdivided into four informal units,among which Units 2 and 3 show the main ichnological content that documents the development of a low diversity trace-fossil assemblage, materialised by

Chondrites intricatus, Ophiomorpha isp., Planolites isp., Thalassinoides isp., Zoophycos brianteus, and Zoophycos cauda-galli, among which Zoophycos and Chondrites are the most common ichnogenus in the section, thus expressing the development of the Zoophycos ichnofacies, which classically reflects a relatively stable outer shelf environment below storm wave base.It corresponds to the lower offshore to shelf edge environments, in which the low sedimentation rate,oxygenation (aerobic and dysaerobic conditions), and high benthic food content are the most important palaeoecological characteristics that control the development of Zoophycos specimens.Consequently,the shallow-tier medium-to-large J-shaped coiled Zoophycos suggests a low sedimentation rate with a significant high oxygenation (aerobic condition) amount,which promotes the accumulation of huge amounts of benthic food,thereby allowing Zoophycos-organisms to explore large surfaces of the substrate efficiently.Thus,it is characterized by the highest bioturbation intensity and the large Zoophycos recognized for the Oued Fodda Formation.On the other hand, despite the low sedimentation rate in a quiet and stable environment,the upper part of Unit 2 is characterized by stressful and dysoxic conditions,which could have stressed the mudfeeding organisms; therefore, a small coiled to U-shaped Zoophycos were produced within the low diversity trace-fossil assemblage.The improved oxygenation towards Unit 3 allows the benthic animals to produce medium- to large-sized traces at another time.The different development of the trace-fossil assemblage assigned to the Zoophycos ichnofacies in the Oued Fodda Formation with different bioturbation intensity, and tiering within Zoophycos-,Planolites-,and Chondritesbearing levels seems to be strongly influenced by the low sedimentation rate and the oxygenation amounts in a mud-rich substrate of quiet and stable environment.

Funding

This work was supported by the General Directorate of Scientific Research and Technological Development“DGRSDT” (Algeria) to Imad Bouchemla and Madani Benyoucef,and by the Fundamental Research Funds for the Universities of Henan Province (NSFRF200340) and the Program for Innovative Research Team (in Science and Technology) of Henan Polytechnic University(T2022-5)to Li-Jun Zhang,and by“Ma?e Projekty 2022”(Faculty of Natural Sciences, University of Silesia in Katowice)to Mariusz A.Salamon.

Availability of data and materials

Data supporting the findings of this study are available upon request from the corresponding authors Imad Bouchemla and Li-Jun Zhang.

Authors'contributions

Imad Bouchemla and Li-Jun Zhang conceived and designed the study, collected and analysed data, and wrote the original draft.Madani Benyoucef and Mariusz A.Salamon read the manuscript, performed the experiment and field job.All authors read and approved the final manuscript.

Conflicts of interest

The authors declare that they have no competing interest.

Acknowledgements

The authors thank the anonymous reviewers and the editors for their valuable comments and suggestions that improved the manuscript.We would like also to thank Prof.Mouley Charaf Chabou, Director of the Architecture and Earth Sciences Institute, Ferhat Abbas University of S′etif, for his generosity and approval for the confection of thin sections in the Department of Earth Sciences.