Spreite and nonspreite burrows

An ethologically and ichnotaxonomically important feature of some trace fossils is a spreite, which is widely regarded by ichnologists as a site of reworked sediment consisting of closely spaced tunnel walls that were packed together as the burrow tunnel was repeatedly shifted laterally (broadside) through the sediment (Seilacher, Reference Seilacher1964, Reference Seilacher2007; Frey, Reference Frey1973; Häntzschel, Reference Häntzschel1975; Ekdale et al., Reference Ekdale, Bromley and Pemberton1984; Bromley, Reference Bromley1996; Buatois and Mángano, Reference Buatois and Mángano2011; Rindsberg, Reference Rindsberg2012; Uchman and Wetzel, Reference Uchman and Wetzel2012). The behavioral significance of a spreite is that it represents the continuous activity of a burrower that processes sediment by successively moving its burrow short distances sideways, creating a series of previously occupied, sediment-filled, ghost tunnels compacted side by side in either a protrusive or retrusive direction (i.e., away from or toward the apertures, respectively). The spreite thus represents sediment that was actively reworked by the animal and is not just a passive fill of an open burrow. Rhizocorallium, a well-known ichnogenus in the geologic record, is a predominantly horizontal U-shaped burrow with a distinct spreite located between the two parallel limbs of the U-shaped tunnel (Häntzschel, Reference Häntzschel1975; Schlirf, Reference Schlirf2011; Knaust, Reference Knaust2013). Although the U-shaped burrows at Alcoi were assigned to Rhizocorallium Zenker, Reference Zenker1836 by Gibert (Reference Gibert2011), it is clear that they do not contain a spreite. Instead, the Alcoi burrows are tongue-shaped slots that were passively filled by sediment that exhibits no evidence of biogenic reworking. The originally open nature of these tongue-shaped burrows is clearly evidenced by three crucial observations: (1) the clear-cut bioglyphs on the interior burrow margins, (2) the passively compacted sediment in the central part of the ‘tongue,’ and (3) the occurrence of barnacles attached to the interior of margins of the burrow. Łomnicki (Reference Łomnicki1886) appropriately assigned these burrows to Glossifungites saxicava, which is not a spreiten burrow. The ichnogenus Glossifungites therefore is not the same as Rhizocorallium. Despite some published opinions to the contrary (Fürsich, Reference Fürsich1974b; Knaust, Reference Knaust2013), Glossifungites is not a synonym of Rhizocorallium; it stands apart as a valid ichnogenus, to which the tongue-shaped burrows at Alcoi are appropriately assigned.

Tracemakers

Spongeliomorpha burrow systems, characterized by the presence of bioglyphs, commonly are attributed to the burrowing activity of decapod crustaceans (e.g., Fürsich, Reference Fürsich1973; Seilacher, Reference Seilacher2007). Burrowing activity of modern crustaceans is well known, especially by decapods such as thalassinidean and alpheid shrimps, astacideans (lobsters and crayfish) and brachyuran crabs, or by other kinds of crustaceans such as stomatopods (mantis shrimps) (Atkinson and Taylor, Reference Atkinson and Taylor1988; Atkinson et al., Reference Atkinson, Froglia, Arneri and Antolini1997). Gibert and Ekdale (Reference Gibert and Ekdale2010), based on a detailed study of the Miocene S. iberica from Muela de Maraón (Murcia, SE Spain), proposed thalassinidean and alpheid shrimps as the possible tracemakers of S. iberica since these kinds of crustaceans generate today geometrically complex burrow systems with turnarounds and chambers very similar to those of this ichnotaxon.

Seilacher (Reference Seilacher2007), Ekdale and Gibert (Reference Ekdale and Gibert2010), and Gibert and Ekdale (Reference Gibert and Ekdale2010) interpreted three burrowing behaviors from the three different bioglyphs present in Spongeliomorpha: (1) Y-shaped ridges were interpreted as the plucking action of the chelipeds and mainly related to digging ahead, (2) long longitudinal ridges were attributed to pereiopods widening the tunnel, and (3) shorter, transverse ridges were related to the ventilation tasks carried out by uropods or to the gnawing of maxillipeds or other mouth parts to graze on bacterial film located in the tunnel wall. In the S. iberica of Alcoi, only those interpreted as produced by chelipeds and very rarely by pereiopods have been identified.

Glossifungites was first interpreted by Łomnicki (Reference Łomnicki1886) as borings produced by lithophagous sponges and subsequently filled by coarse sands. However, despite the fact that G. saxicava sometimes has been referred to as R. jenense, this ichnotaxon commonly has been attributed to the burrowing activity of crustaceans (see Knaust, Reference Knaust2013 and references therein). In addition, Knaust (Reference Knaust2013) proposed chewing annelids as possible producers. However, as with Spongeliomorpha, the presence of different bioglyphs would support the proposal according to which an animal (very likely a crustacean) with rigid appendages capable of scratching the firm mud in different ways was the tracemaker. By contrast, it would be expected that the bioglyphs produced by annelid jaws (see Knaust, Reference Knaust2013) would be more repetitive (with a unique morphology) and smaller than those observed in the G. saxicava of Alcoi. The modern amphipod Corophium excavates U-shaped burrows and frequently has been suggested as a possible analogue of the Rhizocorallium tracemaker (Gibert, Reference Gibert2011). However, the tongue-shaped morphology of Glossifungites has not been observed in modern amphipod burrows or in other kinds of crustacean burrows. Nevertheless, this tongue-shaped architecture also might correspond to the slightly different burrowing behavior of amphipods adapted to colonizing firm substrates.

In the Miocene outcrop at Can Pardinetes, it is possible to observe a continuous gradation of sizes in Glossifungites specimens (Fig. 2), all of them sharing identical morphological features. This would suggest the presence of different ontogenetic stages and hence the coexistence of juvenile and adult individuals of the same species in the same sedimentary horizon.

As stated, Gastrochaenolites generally is defined as clavate (club-shaped) borings produced by bivalves in hard substrates (e.g., Bromley, Reference Bromley2004). However, it is known that traces with identical morphology can be produced in softer materials and preserved in the lithified record (Savazzi, Reference Savazzi1999; Belaústegui et al., Reference Belaústegui, Gibert, de, Nebelsick, Domènech and Martinell2013). An identical morphology enables the use of the same ichnotaxonomic nomenclature, despite the different original substrate. In the Miocene outcrop of Can Pardinetes, the origin of these structures is attributed to the activity of a bivalve, very likely belonging to the pholadid genus Barnea. In one Gastrochaenolites specimen, the shell of the tracemaker is partially exposed in the base of the boring (Fig. 4.4). A finely cancellate sculpture is visible, but there are no more traits to permit a more accurate identification. Some bivalve internal molds also have been collected, corresponding to sediment infills of closed shells. Presumably they also represent shells of the borers, but the absence of identifying features of a pholadid has impeded a more accurate identification.

Cryptobionts

Morton and Challis (Reference Morton and Challis1969) utilized the term ‘cryptobion’ to designate communities enclosed within living or dead coral and revealed only by cracking the substratum, thus distinguishing between pioneering species that bore or excavate galleries and secondary species that nestle or take refuge in those galleries abandoned by the pioneers. In the same sense as these authors, Shirayama and Horikoshi (Reference Shirayama and Horikoshi1982) used the term ‘cryptobionts’ to divide these secondary species in two groups: mobile species that utilize natural interstices and or biogenic crevices or holes in the coral skeleton, and immobile species that are embedded passively in the coral skeleton by coral growth.

In studying marine boring microorganisms, Golubic et al. (Reference Golubic, Perkins and Lukas1975) differentiated among ‘epiliths’ (living on the surface of the substrate), ‘chasmoliths’ (adhering to the surfaces of fissures and cavities within the substrate), and ‘endoliths’ (penetrating into the substrate). Subsequently, Golubic et al. (Reference Golubic, Friedmann and Schneider1981) redescribed ‘endoliths’ as colonizers of the interior of rocks, and he divided them into ‘chasmoendoliths’ (colonizers of clefts in the rock), ‘cryptoendoliths’ (hidden colonizers of structural cavities within porous rocks, including spaces produced and vacated by euendoliths), and ‘euendoliths’ (rock-boring organisms).

Finally, Kobluk (Reference Kobluk1988b) proposed a uniform terminology to designate cryptic marine organisms inhabiting reefs and other settings. Among other terms, Kobluk (Reference Kobluk1988b) defined ‘cryptobiont’ as “an individual organism or species within the cryptos, or living in a crypt”; ‘crypt’ as “general term to refer to the habitats within all kinds of cavities or completely or partially enclosed void spaces”; ‘cryptos’ as “organisms as a group with a hidden mode of life living protected from full or direct exposure to major physical environmental factors”; and ‘cryptic’ as “adjective referring to organisms belonging to the cryptos” (p. 381, table 1). Kobluk’s terminology is followed in this manuscript.

Cryptobionts are common in the fossil record. In the review of pre-Cenozoic cryptobionts associated with reefs and mounds that was offered by Kobluk (Reference Kobluk1988a), the oldest occurrences date back to the Cambrian and Ordovician (see also Hong et al., Reference Hong, Choh and Lee2014). To a lesser extent, even the activity of infaunal soft- and mainly hard-substrate cryptobionts is known in marine paleoenvironments (see Uchman et al., Reference Uchman, Mikuláš and Houša2003 and references therein). Today, the most common organisms with cryptic habits are algae, foraminifera, sponges, corals, polychaetes, mollusks, bryozoans, and brachiopods (Kobluk and Lysenko, Reference Kobluk and Lysenko1993; Lukeneder and Harzhauser, Reference Lukeneder and Harzhauser2003; Taylor and Wilson, Reference Taylor and Wilson2003; Zuschin and Mayrhofer, Reference Zuschin and Mayrhofer2009; Schlagintweit and Bover-Arnal, Reference Schlagintweit and Bover-Arnal2012).

In the Miocene outcrop of Can Pardinetes, it is possible to observe calcareous basal plates of balanomorph barnacles (Crustacea: Cirripedia: Thoracica) in the outer surface of several Glossifungites and Spongeliomorpha specimens (Fig. 6), but never on Gastrochaenolites traces. Thin sections clearly show that the basal plates of these barnacles are attached directly to the walls of the burrows since they are associated with the wall plates, which are preserved in their original life position inside the burrow infills (Fig. 7). Occasionally, opercular plates also have been observed inside the barnacle shells (Fig. 7.1). There is no doubt that these barnacles colonized the interiors of the burrows by attaching to the burrow walls, and therefore they can be regarded as cryptobionts. The total number of clustered barnacles in Glossifungites specimens is variable (from 3 to 41), and the diameter of basal plates varies from 3.7 to 10.3 mm. In Spongeliomorpha, basal plates range from 2.4 to 8.2 mm, with clusters of up to 14 barnacles. Maximum observed height is 2 mm. A. dolosus is a thoracican cirripede species that is present in the European Neogene, including the middle Miocene of France (Davadie, Reference Davadie1963) and Pliocene of the United Kingdom (Darwin, Reference Darwin1854; Menesini, Reference Menesini1964; Newman et al., Reference Newman, Zullo and Withers1969). This paper reports its first record of occurrence in cryptic environments.

Although the presence of cryptobionts inhabiting the inside of hardgound burrow systems (mainly Thalassinoides-like) is well documented (e.g., Fürsich and Palmer, Reference Fürsich and Palmer1975; Voigt, Reference Voigt1987, Reference Voigt1988; Wilson and Taylor, Reference Wilson and Taylor2001), only once before now has the presence of cryptobionts attached to the inner walls of noncemented burrows been described in the fossil record, in particular foraminifera (but not barnacles) within Thalassinoides burrows in the Upper Cretaceous of the Netherlands (Hofker, Reference Hofker1965). Furthermore, the occurrence of cirripeds in other fossil cryptic environments (e.g., caverns, grooves, crevices, or hidden spaces between cobbles or boulders) is not widely documented. Aguirre et al. (Reference Aguirre, Belaústegui, Domènech, Gibert and Martinell2014) described the presence of balanoid (Balanus trigonus Darwin, Reference Darwin1854) and pyrgomatid (Pyrgoma sp.) barnacles inhabiting grooves and crevices of a Pliocene Dendropoma reef from the Baix Ebre Basin (NE Spain). Rosso et al. (Reference Rosso, Sanfilippo, Ruggieri, Maniscalco and Vertino2015) recorded the occurrence of the barnacles Balanus perforatus Bruguière, Reference Bruguière1789 and Verruca spengleri Darwin, Reference Darwin1854 in a Pleistocene submarine cave in Sicily (Italy). Scarce examples of bioerosion structures attributed to the boring activity of acrothoracican barnacles (ichnogenus Rogerella) also have been recorded in fossil cryptic settings (Palmer and Fürsich, Reference Palmer and Fürsich1974). Today, such genera as Amphibalanus, Chthamalus, and Euraphia (Balanomorpha) are common inhabitants in grooves and crevices in different locales around the Mediterranean area (Linkin and Safriel, Reference Linkin and Safriel1971; Crisp et al., Reference Crisp, Southward and Southward1981; Guy-Haim et al., Reference Guy-Haim, Rilov and Achituv2015). The species Balanus glandula Darwin, Reference Darwin1854 has been observed colonizing firmgrounds at Willapa Bay, Washington (Gingras et al., Reference Gingras, Pemberton and Saunders2001).

When studying the effect of light on the growth rate of two Balaninae barnacles, Barnes (Reference Barnes1952 and references therein) concluded that wave action and water flow is much more important on the barnacle growth than the effect of light, which is almost insignificant. This fact could indicate that the barnacles colonized the interior of the burrows while these were still occupied by their producers, likely alpheid or thalassinidean shrimps (at least in the case of Spongeliomorpha burrow systems), since it is known that these kinds of decapod crustaceans, by pleopod beating, pump oxygen-rich surface water through their burrows promoting good irrigation and ventilation (Dworschak, Reference Dworschak1981; Forster and Graf, Reference Forster and Graf1995; Astall et al., Reference Astall, Taylor and Atkinson1997; Stamhuis and Videler, Reference Stamhuis and Videler1998a, Reference Stamhuis and Videlerb, Reference Stamhuis and Videlerc; Atkinson and Taylor, Reference Atkinson and Taylor2005). In addition to this, some thalassinidean shrimps collect and accumulate organic debris material as a food source in the walls or in chambers of their burrows, and these actions may increase the amount of organic content and bacteria in deeper layers of the sediment (Branch and Pringle, Reference Branch and Pringle1987; Dworschak, Reference Dworschak2001; Dworschak et al., Reference Dworschak, Koller and Abed-Navandi2006). Therefore, since the microhabitat generated within these burrows provides: (1) ventilated and oxygenated waters, (2) high bacterial and organic content, and (3) protection against predators, its colonization by cryptic barnacles seems reasonable. In fact, within the burrows of thalassinidean shrimps, the cohabitation (mainly commensalism) of the producers with different organisms such as other decapods (e.g., alpheid shrimps), amphipods, bivalves, polychaetes, or even gobiid fish have been described both in the fossil record and today (Dworschak et al., Reference Dworschak, Anker and Abed-Navandi2000; Anker et al., Reference Anker, Jeng and Chan2001; Kneer et al., Reference Kneer, Asmus and Vonk2008; Liu et al., Reference Liu, Kneer, Asmus and Ahnelt2008; Nara et al., Reference Nara, Akiyama and Itani2008).

Depositional sequence

The Can Pardinetes outcrop exemplifies several successive colonization stages of an exposed sea floor during the middle to upper Miocene (Langhian-Tortonian), which are represented by a succession within the same ichnocoenose (Fig. 5). The sequence stratigraphic implications suggest a regressive trend with submarine exposure during a sea level lowstand.

First, marly lime sediment was deposited under shallow subtidal marine conditions, and the seafloor was occupied by a benthic fauna, which presumably contributed a preomission suite of trace fossils, which could not be observed in the field during this study due to poor preservation. Then the water shallowed, and sedimentation apparently ceased (with or without erosional events). The seafloor became compacted and firm, creating a firmground omission surface that was occupied by burrowers capable of penetrating the stiff (but uncemented) sediment.

The omission suite of trace fossils includes tongue-shaped burrows (Glossifungites saxicava), branching burrow systems (Spongeliomorpha iberica), and club-shaped dwellings (Gastrochaenolites ornatus) that were produced contemporaneously by probably two taxa of crustaceans and one of pholadid bivalves. The three types of trace fossils clearly are connected in some specimens, testifying to their contemporaneity and the high bioturbation intensity at that time. In some cases it is possible to observe Glossifungites specimens that were colonized by the tracemaker of Spongeliomorpha, which partially adapted its burrow to the previous one (Fig. 2.4) or just cut across it (Figs. 2.1, 3.6). The latter case also occurred between Gastrochaenolites and Spongeliomoprha in some specimens (Fig. 4.1). This ichnocoenose was repeated at least two times due to successive erosive events (Fig. 5.2).

These trace fossils constitute a typical firmground ichnoassemblage of the Glossifungites ichnofacies as described by Seilacher (Reference Seilacher1967; Pemberton and Frey, Reference Pemberton and Frey1985). Glossifungites ichnofacies dominated by the ichnospecies G. ornatus, as occur in the Miocene of Alcoi, also have been described in the Miocene of Patagonia, Argentina (Carmona et al., Reference Carmona, Mángano, Buatois and Ponce2007). In firmgrounds at Willapa Bay (Washington, USA), Gingras et al. (Reference Gingras, Pemberton and Saunders2001) described modern Glossigungites ichnofacies trace assemblages that are dominated by the burrows of bivalves (genus Petricola) and decapod crustaceans (genus Upogebia), which generate Gastrochaenolites- and Thalashinoides-like structures, which share a lot of similarities with the Miocene case studied here.

Cryptic barnacles could have colonized the inner walls of Spongeliomorpha and Glossifungites burrows while these were still occupied by their producers, thus benefiting from the benign and protected microhabitats generated by some kinds of crustaceans within their burrows (see section ‘Cryptobionts’). Conversely, these burrows could have been colonized after being abandoned and before being filled by sediment. In either case, barnacles are mostly attached to the roofs of the more horizontally disposed burrows. This preference for the roof of the burrow over the bottom could be explained by: (1) the presence of loose sediment deposited passively in the bottom, which could prevent their attachment and their breathing; (2) avoiding trampling by the host; or (3) a greater degree of compaction of the roof than the bottom. In fact, the preservation of bioglyphs also is generally better on the roof than on the bottom.

Some specimens, mainly those belonging to Glossifungites and Spongeliomorpha, exhibit irregular cavities (Figs. 2.2, 3.2). Thin section evidence rules them out as bioerosion structures, since any clasts in their outer perimeter show no evidence of having been cut or dissolved. Irregular rounded marl clasts have been observed within many specimens (e.g., Fig. 4.7). Since they have the same lithology as those of the surrounding white marls (Tap), they can be considered as mud clasts. The origin of these mud clasts is due to erosional and transport processes and may be related to shrinkage and cracking of mud layers as well as to erosion and reworking by high-energy events (Knight, Reference Knight2005; Ghandour et al., Reference Ghandour, Al-Washmi and Haredy2013 and references therein). The marly firm substrate that constituted the seafloor in Alcoi was exposed by at least one erosional event, as evidenced by the record of two omission suites of firmground burrows. During the erosive process, the marly firm substrate may have become fragmented and some of these fragments were redeposited as marl clasts. Some marl clasts fell into the open trace fossils, were deposited by gravity on their bottoms, and finally were buried by the passive infilling of these trace fossils by a fine-grained quarzitic calcareous sand. After diagenesis, burrow casts were totally hardened and cemented as calcarenite. Once this bioturbated unit was exposed to weathering, the differential erosion of looser marly sediments, including the marl clasts located in the outer part of the trace fossils, promoted the formation of these irregular cavities in the burrow casts.