Fossil sponges have a complicated taxonomy that has fundamental issues yet to be resolved, for example: relationships among main sponge clades are still uncertain, and fossil and recent classification proposals proved difficult to integrate – some morphological grades occur across different orders (e.g., Wood Reference Wood1990; Senowbari-Daryan & García-Bellido Reference Senowbari-Daryan, García-Bellido, Hooper and Van Soest2002; Finks & Rigby Reference Finks, Rigby and Kaesler2004; Pisera Reference Pisera2006; Vacelet et al. Reference Vacelet, Willenz and Hartman2010). Many species are difficult to classify without thorough observation of very specific traits, some of which require extensive sectioning of specimens and scanning electron microscope (SEM) imaging (Wood Reference Wood1990; Díaz & Rützler Reference Díaz and Rützler2001). In the last few decades many advances have been made for extant sponges, through DNA sequencing analyses and cladistic approaches (e.g., Morrow & Cárdenas Reference Morrow and Cárdenas2015). Fossil sponges are even more difficult to identify as biostratinomy and diagenesis often obliterate or alter diagnostic skeletal features (Wood Reference Wood1990; Pisera Reference Pisera2006; Wulff Reference Wulff2006). Thus, the fossil record is strongly biased towards sponges with a rigid mineralised skeleton (Pisera Reference Pisera2006). The plasticity of sponge growth is another factor that complicates taxonomic assignment of fossils, as the same taxon can vary substantially in shape among different environmental settings (e.g., Palumbi Reference Palumbi1984; Loh & Pawlik Reference Loh and Pawlik2009; Ávila & Ortega Bastida Reference Ávila and Ortega Bastida2014). In addition, fossil sponges are truly rare in some rocks and time intervals (Pisera Reference Pisera2006).
However, the various ecological functions of sponges and their importance have been acknowledged in the literature on both fossil and extant forms (e.g., Wood Reference Wood1990; Díaz & Rützler Reference Díaz and Rützler2001; Wulff Reference Wulff2006; Bell Reference Bell2008). Since the Cambrian, sponges have been reef-builders with different taxonomic groups dominating this niche over the Phanerozoic (see Brunton & Dixon Reference Brunton and Dixon1994; Pisera Reference Pisera2006; Wulff Reference Wulff, Hubbard, Rogers, Lipps and Stanley2016; Maldonado et al. Reference Maldonado, Aguilar, Bannister, Bell, Conway, Dayton, Díaz, Gutt, Kelly, Kenchington, Leys, Pomponi, Rapp, Rützler, Tendal, Vacelet, Young, Rossi, Bramanti, Gori and Orejas Saco del Valle2017). From the Mesozoic onwards, sponges became important binders as well as playing parts in stabilisation, consolidation and regeneration of reef frames (Bell Reference Bell2008; Wulff Reference Wulff, Hubbard, Rogers, Lipps and Stanley2016). In deeper settings, hexactinellid mounds and reefs persist even today, and they represent biodiversity hotspots in such environments (Kauffman et al. Reference Kauffman, Herm, Johnson, Harries and Höfling2000; Maldonado et al. Reference Maldonado, Aguilar, Bannister, Bell, Conway, Dayton, Díaz, Gutt, Kelly, Kenchington, Leys, Pomponi, Rapp, Rützler, Tendal, Vacelet, Young, Rossi, Bramanti, Gori and Orejas Saco del Valle2017). Recent sponges are also important components of mangroves and seagrass meadows (e.g., Diaz Reference Diaz, Maldonado, Turon, Becerro and Jesús Uriz2012; Ávila & Ortega Bastida Reference Ávila and Ortega Bastida2014; Maldonado et al. Reference Maldonado, Aguilar, Bannister, Bell, Conway, Dayton, Díaz, Gutt, Kelly, Kenchington, Leys, Pomponi, Rapp, Rützler, Tendal, Vacelet, Young, Rossi, Bramanti, Gori and Orejas Saco del Valle2017). Boring sponges play a significant part in carbonate cycling by breaking up calcareous materials and clasts (Rützler Reference Rützler1975; Achlatis et al. Reference Achlatis, van der Zande, Schönberg, Fang, Hoegh-Guldberg and Dove2017). Sponge communities have an impact on the water column as well (bentho-pelagic coupling), playing important roles in the carbon, nitrogen, oxygen and silica cycles (see Bell Reference Bell2008) and maintaining water clarity (Wulff Reference Wulff, Hubbard, Rogers, Lipps and Stanley2016); they also contribute significantly to the removal of bacteria and other microorganisms through their filtering activity (Díaz & Rützler Reference Díaz and Rützler2001; Bell Reference Bell2008). They provide nourishment for many different types of consumers (see Wulff Reference Wulff2006; Maldonado et al. Reference Maldonado, Aguilar, Bannister, Bell, Conway, Dayton, Díaz, Gutt, Kelly, Kenchington, Leys, Pomponi, Rapp, Rützler, Tendal, Vacelet, Young, Rossi, Bramanti, Gori and Orejas Saco del Valle2017). A great variety of single-celled autotrophs and heterotrophs dwell within sponge tissues (see Wulff Reference Wulff2006; Taylor et al. Reference Taylor, Radax, Steger and Wagner2007, for an overview). In addition, sponges often establish remarkably diverse symbiotic associations with a variety of algae, invertebrates (including crustaceans, bryozoans, polychaetes, ophiuroids, cnidarians and molluscs) and fishes (Wulff Reference Wulff2006, Reference Wulff, Hubbard, Rogers, Lipps and Stanley2016 and citations therein). Besides they may also host a diverse sclerobiont fauna, resulting in increased local benthic diversity (e.g., Gundrum Reference Gundrum1979; Wilson et al. Reference Wilson, Feldman, Bowen and Avni2008, Reference Wilson, Feldman and Belding Krivicich2010).
Despite their importance, studies on fossil sponges that focus on their ecological roles are generally rare (Pisera Reference Pisera2006), particularly for Mesozoic sponges (e.g., Palmer & Fürsich Reference Palmer and Fürsich1981; Fürsich & Werner Reference Fürsich and Werner1991; Werner et al. Reference Werner, Leinfelder, Fürsich and Krautter1994; Leinfelder Reference Leinfelder1992). Lithistid and hexactinellid sponge-dominated reefs were quite common during the Jurassic–Cretaceous, and thus are extensively studied (see Maldonado et al. Reference Maldonado, Aguilar, Blanco, García, Serrano and Punzón2015, and citations therein). Sponges also took part in other types of reefs or mounds; for some examples consult Palmer & Fürsich (Reference Palmer and Fürsich1981), Fürsich & Werner (Reference Fürsich and Werner1991), Leinfelder (Reference Leinfelder1992), Kauffman et al. (Reference Kauffman, Herm, Johnson, Harries and Höfling2000), Svennevig & Surlyk (Reference Svennevig and Surlyk2019) and Bonuso et al. (Reference Bonuso, Stone and Williamson2020). Most studies deal with Jurassic or Late Cretaceous occurrences centred mostly in Europe, with few mentions of Early Cretaceous records.
Argentinian fossil sponges are quite common and abundant in Palaeozoic successions (e.g., Carrera Reference Carrera1997a, Reference Carrerab, Reference Carrera and Benedetto2003; Beresi Reference Beresi, Custódio, Lôbo-Hadju, Hadju and Muricy2007; Beresi & Rigby Reference Beresi and Rigby2013; Carrera et al. Reference Carrera, Rustán, Vaccari and Ezpeleta2018), but Mesozoic records are scarce (e.g., Afᶊar et al. Reference Afşar, Duda, Zeller, Verwer, Westphal and Eberli2014). A remarkable exception is that of the Oxfordian La Manga Formation reefal structure, which bears a moderately diverse siliceous sponge assemblage, that occurs in the mainly coral-built structure (Beresi Reference Beresi, Custódio, Lôbo-Hadju, Hadju and Muricy2007). In the Lower Cretaceous Agrio Formation (AF) fossil sponges have been mentioned or figured but never studied in detail. Small sponges are usually found attached to ramose coral colonies in shallow water coral patch-reefs and coral meadows (e.g., Lazo et al. Reference Lazo, Cichowolski, Rodríguez, Aguirre-Urreta, Veiga, Spalletti, Howell and Schwarz2005; Garberoglio et al. Reference Garberoglio, Lazo and Palma2013; Luci et al. Reference Luci, Garberoglio, Manceñido and Lazo2015; Garberoglio Reference Garberoglio2019); alternatively loose siliceous spicules have been described from thin sections of fine grained carbonates from distal marine settings (see Sagasti & Ballent Reference Sagasti and Ballent2002). In addition, borings on mollusc shells and corals, usually referred to clionid sponges were described (see Garberoglio et al. Reference Garberoglio, Lazo and Palma2013; Garberoglio Reference Garberoglio2019; Toscano et al. Reference Toscano, Luci, Cataldo and Lazo2021). In this paper a newly discovered sponge meadow from the AF is reported for the first time. The objectives of the present paper are as follows: (a) to describe and identify these sponges to the lowest taxonomic level possible; (b) to analyse their sclerobiont community, including sclerobiont taxa identification, interactions among them and with the sponges and other palaeoecological metrics; and (c) to interpret the sponge assemblage in palaeoecological terms along with its associated palaeoenvironment, and reconstruct the sponge meadow establishment, climax and demise.
1. Geological setting of the sponge-bearing bed
The Neuquén Basin, located in west-central Argentina, extends through most of the Neuquén and Mendoza provinces along the Andean foothills, between 32° and 40° SL (Fig. 1). During most of Jurassic and Early Cretaceous times it was a retro-arc basin with a gentle thermal subsidence regime. Oceanic waters penetrated from the Pacific Ocean through a volcanic arc to the west and formed a large marine epicontinental embayment. During the Early Cretaceous the basin was located not far from its current position, roughly between 28° and 36° SL (Somoza Reference Somoza2011), a mid-latitudinal location at the boundary between the tropical and subtropical belts.
Figure 1 (a) Map showing the former location and shape of the Neuquén Basin for the Early Cretaceous, and the main (north) and Picún Leufú (south) depocentres separated by the Huincul High. (b) Geological map of the study area, with the main outcropping units.
The materials studied here come from the Picún Leufú depocentre, which developed in the southern region of the basin, between the Huincul High to the north and the North Patagonian Massif to the south (Fig. 1). The Huincul High, an east–west oriented morphostructural feature, was proved to be an ancient positive element developed since Early Jurassic times prior to the main Andean contractional cycle that started in the Late Cretaceous (Ramos et al. Reference Ramos, Folguera, García Morabito, Leanza, Arregui, Carbone, Danieli and Vallés2011; Naipauer et al. Reference Naipauer, García Morabito, Marques, Tunik, Rojas Vera, Vujovich, Pimentel and Ramos2012). This topographic high was at times a true division between the northern and southern regions of the basin, especially during times of relative sea level fall, but during transgressive episodes, marine waters drowned it and both regions became partially connected. It is within this southern depocentre that the studied sponge meadow was recorded in the AF.
The AF, defined by Weaver (Reference Weaver1931), is a well-known unit because of its abundant and diverse marine fossil content and also because it is a reservoir unit of interest for oil exploitation. It was deposited from early Valanginian to latest Hauterivian times based on a refined ammonoid biostratigraphy which has been correlated to the European Standard Ammonoid Zonation and constrained by precise radioisotopic dates (see Aguirre-Urreta et al. Reference Aguirre-Urreta, Mourgues, Rawson, Bulot and Jaillard2007, Reference Aguirre-Urreta, Schmitz, Lescano, Tunik, Rawson, Concheyro, Buhler and Ramos2017, Reference Aguirre-Urreta, Martinez, Schmitz, Lescano, Omarini, Tunik, Kuhnert, Concheyro, Rawson, Ramos, Reboulet, Frederichs, Nickl and Pälike2019). The unit comprises three members: the lower Pilmatué Member; the middle Avilé Member; and the upper Agua de la Mula Member (Weaver Reference Weaver1931; Leanza et al. Reference Leanza, Hugo and Repol2001). The upper and lower members are marine, representing inner to outer ramp settings with abundant benthic fauna (e.g., Lazo Reference Lazo2007a). In the Picún Leufú depocentre, the unit overlies the Bajada Colorada Formation and underlies the La Amarga Formation, and the Avilé Member is not recorded. The unit is well exposed at several localities that are easily correlated among each other due to an abundant and diverse macrofossil and microfossil content (see Musacchio & Simeoni Reference Musacchio and Simeoni2008; Cataldo & Lazo Reference Cataldo and Lazo2012; Luci & Lazo Reference Luci and Lazo2015). In terms of facies, the unit is composed mainly of carbonate shales alternating with shell beds, skeletal sandstones, packstones and grainstones (di Paola Reference Di Paola1990).
The studied sponges were collected at Cerro Marucho (S 39°25.71′; W70°10.173′). This locality lies on a prominent hill next to National Road 40, some 60 km south of Zapala City, Neuquén Province. Here, the AF is well exposed, and a detailed sedimentary log of 127 m was made (Fig. 2; see also Leanza & Hugo Reference Leanza and Hugo1997; Musacchio & Simeoni Reference Musacchio and Simeoni2008; Lescano & Concheyro Reference Lescano and Concheyro2014). The sponge-bearing level was recorded within the Hoplitocrioceras gentilii Zone of Early Hauterivian age, that in turn has been correlated with the Lyticoceras nodosoplicatum Mediterranean Standard Zone (see Aguirre-Urreta et al. Reference Aguirre-Urreta, Mourgues, Rawson, Bulot and Jaillard2007; Reboulet et al. Reference Reboulet, Szives, Aguirre-Urreta, Barragán, Company, Idakieva, Ivanov, Kakabadze, Moreno-Bedmar, Sandoval, Baraboshkin, Çaglar, Fözy, González-Arreola, Kenjo, Lukeneder, Raisossadat, Rawson and Tavera2014).
Figure 2 Measured section at Cerro Marucho. To the left, a generalised stratigraphic column of the Agrio Formation is shown; to the right, the partial section of the Pilmatué Member measured in Cerro Marucho is depicted, with the sponge meadow level indicated by an arrow.
The studied sponge bed corresponds to a single lenticular bed of poorly consolidated grey marlstone of 1.8 m of maximum thickness and 20 m of maximum width along strike. This lens is embedded in a 30 m-thick continuous interval of tabular grey shales with abundant ammonoids lying parallel to the bedding planes (Fig. 2). The lens contains abundant sponges, loosely packed (no contact among bioclasts). At its base is an oyster shell bed composed of small cementing Ceratostreon exogyrid oysters, that grades upwards into sponge-bearing marls. Sponge specimens are placed mostly above the oyster shell bed: a gradual increase in sponge abundance was detected towards the top. Abrasion and/or rounding were negligible for both sponges and oysters. Sponges and oysters were oriented parallel to bedding in cross-section and randomly in a plane view. No other benthic macrofauna was observed, except for the sclerobionts harboured by the sponges (see section 3). Base contact was sharp and top contact gradational. No sedimentary structures were recorded and both surfaces that limit the lenticular sponge-bearing bed cannot be traced laterally beyond the lens, that is, they have no great local, much less regional importance. Thus, the lens is a very local, within facies occurrence, as both below and above it, grey shales with scattered ammonites occur. This is also supported by the fact that the sponge bed was not recorded in nearby localities such as Cerro Birrete and Cerro Negro Chico de Picun Leufú. A distal low energy ramp setting is envisaged with a predominance of settling of suspended fine-grained carbonates.
The sponges are interpreted to have formed a low-relief, low-diversity meadow of rare outcrop occurrence. For this definition we followed Aretz (Reference Aretz2010) who defined a series of terms based on coral build-ups in which colonisation of the seafloor varied between high-diversity dense populations and impoverished occurrences.
2. Materials and methods
Sponges were collected in situ from the sponge-bearing level at Cerro Marucho along its field exposition. A total of 137 specimens were examined in detail. They are all deposited in the Museo Olsacher (Zapala City, Neuquén, Argentina) under repository number MOZ-Pi 12114.1-137 (suffix number indicates an individual specimen's number). Finks & Rigby (Reference Finks, Rigby and Kaesler2004) and Senowbari-Daryan et al. (Reference Senowbari-Daryan, Fürsich and Rashidi2020) were followed in the taxonomic section. For general sponge terminology, Webby et al. (Reference Webby, Debrenne, Kershaw, Kruse, Nestor, Rigby, Senowbari-Daryan, Stearn, Stock, Vacelet, West, Willenz, Wood and Zhuravlev2010) were followed. Some specimens were sectioned and polished along the transversal and longitudinal planes in order to observe their inner structure.
Most specimens are terminal branch fragments (with the apical osculum preserved); only six specimens are complete. However, it was evident in field observations that fragmentation was recent, and not caused by extensive reworking of the materials. For all specimens, maximum preserved length and width were measured with a digital caliper.
Prior to data collection, sponges were washed under running water with a brush; care was taken that this did not affect (efface or remove) the more delicate sclerobionts by checking on the sponges under a binocular stereomicroscope (up to 50X; Leica EZ5) before and after washing. Little sediment remained attached to the sponges, so there was no need for further cleaning by mechanical means. All cleaned and dried specimens were observed under binocular stereomicroscope and sclerobiont presence/absence data were recorded for each sponge specimen. Interactions among sclerobionts and/or sclerobionts–basibiont were also recorded. Sponges lacking sclerobionts were also accounted for. When present, markings on the sponge skeleton were also recognised. When preserved, the substrate that sponges had settled upon was also recorded. Four specimens (MOZ-Pi 12114.14, 12114.17, 12114.22 and 12114.51) were examined using a SEM for imaging and energy dispersive spectroscopy (EDS) analysis.
Overall richness of sclerobiont taxa was calculated for the whole sponge sample, as well as percentage of sponges presenting at least one sclerobiont. In addition, maximum richness per sponge specimen was also calculated. Number of sponges with a given sclerobiont taxon, and the corresponding percentage over the total number of sponges were calculated; these metrics provide information on dispersion of sclerobiont taxa across available sponge substrates regardless of the abundance of each individual sclerobiont taxon. Richness of sclerobionts per sponge was then plotted against sponge maximum length and width, to search for patterns in number of sclerobiont taxa with respect to sponge size. However, since most specimens are fragmentary, these data must be interpreted with caution. Finally, overall trends in sclerobiont location with respect to any preserved anatomical landmarks in sponge specimens (e.g., osculum, growth direction, ridges and inter-branch spaces in sponges, etc.) were recorded qualitatively.
Three specimens were subject to longitudinal cutting in order to observe whether sclerobionts had been bioimmured by the sponge. The specimens selected for cutting showed distinctive morphologies (for example, ridges that had a corkscrew shape over the sponge) that were suggestive of serpulid overgrowth by the sponge.
3. Systematic palaeontology
Class Calcarea Bowerbank Reference Bowerbank1864
Order Stellispongiida Finks & Rigby Reference Finks, Rigby and Kaesler2004
Family Endostomatidae Finks & Rigby Reference Finks, Rigby and Kaesler2004
Genus Endostoma Roemer Reference Roemer1864
Type species: Scyphia foraminosa Goldfuss Reference Goldfuss1829. Posterior designation by de Laubenfels (Reference de Laubenfels and Moore1955).
Diagnosis: Conical–cylindrical, simple but occasionally basally conjoined, small sponges. Deep, central inner tube. Exhalant channels entering the cloaca sub-horizontally, occurring on top surface as radial grooves converging on the osculum. Additional channels essentially in intertrabecular spaces. Lower part may be covered by an imperforate dermal layer. Fibres conformed by very slender, bundled triradiates; paratangential dermal triradiates and tetraradiates may be present or not (modified from Roemer Reference Roemer1864; Hinde Reference Hinde1884; Finks & Rigby Reference Finks, Rigby and Kaesler2004).
Remarks: The genus was created by Roemer (Reference Roemer1864) to group simple, cylindrical sponges with an inner tube (axial spongocoel) and large, lateral openings, from the Cretaceous of Germany. He also created Polyendostoma, which included Endostoma-like sponges that grew joined at the base. Later, Zittel (Reference Zittel1878) erected Corynella to include simple, thick-walled, sometimes joined at the base, cylindrical, globular or clavate sponges of Triassic–Late Cretaceous age and assigned six Triassic, 18 Jurassic and 11 Cretaceous species to Corynella; among the latter were the then existing species of Endostoma and Polyendostoma, now junior synonyms of Corynella.
Later Hinde (Reference Hinde1883) revised Corynella, adding further details to Zittel's (Reference Zittel1878) diagnosis and describing 15 species in varying detail from the Triassic–Cretaceous of several places over Europe; later on, he added five species from the Jurassic of England to the genus (Hinde Reference Hinde1893). As in Zittel (Reference Zittel1878), he included Endostoma within Corynella. Shortly after the revision of Corynella, Hinde (Reference Hinde1884) appointed Scyphia foraminosa Goldfuss Reference Goldfuss1829 as the type species of Corynella.
Hinde (Reference Hinde1893) erected the genus Peronidella, which differs from Corynella in lacking a radial canal system. However, as the development of the channel system can be very variable in Corynella (ranging from nearly inexistent or limited to the basal portion of the sponge, to clearly present), it is not a reliable diagnostic character.
Dieci et al. (Reference Dieci, Antonacci and Zardini1968) separated the Triassic forms from the north of Italy, based on their spherulitic microstructure and grouped them together in the genus Precorynella. Much later, Rigby & Senowbari-Daryan (Reference Rigby and Senowbari-Daryan1996) grouped the Permian and Triassic species lacking spicules in the genus Permocorynella. Thus, only Jurassic–Cretaceous species remained within Corynella.
Finks & Rigby (Reference Finks, Rigby and Kaesler2004) recognised Corynella Zittel as a junior synonym of Endostoma Roemer, on the basis of both genera sharing the type species. Endostoma was thus redefined as a genus comprising only Jurassic and Cretaceous species.
Recently Senowbari-Daryan et al. (Reference Senowbari-Daryan, Fürsich and Rashidi2020) described three species of Endostoma (one new) and gave a list of valid species of the genus, but their list contains some mistakes in names and dates. The revised list is as follows: Endostoma bullata (Étallon Reference Étallon1860); Endostoma clava (Oppliger Reference Oppliger1929); Endostoma costata (Stahl Reference Stahl1824); Endostoma cribrata (Hinde Reference Hinde1893); Endostoma divisa (Müller Reference Müller1984); Endostoma intermedia (Münster Reference Münster and Goldfuss1829); Endostoma langtonensis (Hinde Reference Hinde1893); Endostoma madreporata (Quenstedt Reference Quenstedt1876–78); Endostoma nodosa (Keeping Reference Keeping1883); Endostoma parva (Étallon Reference Étallon1859); Endostoma perplexa (Quenstedt Reference Quenstedt1876–78); Endostoma polonica (Hurcewicz Reference Hurcewicz1975); Endostoma quenstedti (Zittel Reference Zittel1878); Endostoma stellata Senowbari-Daryan et al. Reference Senowbari-Daryan, Fürsich and Rashidi2020; and Endostoma stolata (Zittel Reference Zittel1878).
The only other genus within the family Endostomatidae, Raphidonema Hinde, has a similar structure but is cup-shaped (Finks & Rigby Reference Finks, Rigby and Kaesler2004), so it can be easily distinguished from Endostoma.
Discussion: Most authors citing Endostoma (or more commonly, Corynella) made no descriptions and published no pictures, and mentions are usually at the genus level. Thus, a thorough revision of species and occurrences is necessary, though this is out of the scope of the present work.
To our knowledge, no analyses have been made on the mineral skeleton of Endostoma, but the genus Barroisia Munier-Chalmas (also a Jurassic–Cretaceous calcareous sponge) has a similar structure to Endostoma and was found to bear triactine spicules embedded in a calcareous matrix, and according to some authors (Reid Reference Reid1968; Masse & Termier Reference Masse and Termier1992) these spicules could be siliceous. However, the finding of siliceous materials within their skeletons does not necessarily imply that these sponges secreted siliceous spicules. This could have alternative explanations, for example, incorporation of foreign materials (some extant sponges incorporate loose spicules into their structure); also, infiltration of siliceous spicules belonging to the boring genus Entobia may occur (Reid Reference Reid1968). Thus, the ability of these sponges to secrete siliceous spicules is still not conclusively proven.
Palaeoecological remarks: Discussions of the palaeoecology of the genus in the literature are limited; there is agreement that these sponges are small (up to a few centimetres in height) and, as with most sponges, they tend to prefer low-energy, relatively deep settings and hard substrates (see section 5 for further details).
Endostoma sp. aff. nodosa (Keeping Reference Keeping1883)
Figs 3, 4
Materials: Sponge materials comprise 137 specimens, listed under repository number MOZ-Pi 12114.1-137. All are from one single bed, Hoplitocrioceras gentilii ammonoid Zone, Early Hauterivian, AF, Cerro Marucho, Neuquén, Argentina.
Figure 3 Overall morphology of Endostoma sp. aff. nodosa MOZ-Pi 12114. (a) Lateral view of a group of tubes joined by their bases (specimen 12114.77). (b) Top view of specimen 12114.130 with short globular projections. (c) Lateral view of a finger-like ramose specimen 12114.12. (d) Lateral view of an isolated tube (specimen 12114.2). (e) Lateral view of two tubes united at the base (specimen 12114.79). (f) Lateral view of specimen 12114.105 growing over Ceratostreon sp. oysters and showing globular projections. (g) Top view of specimen 12114.106 with globular projections. (h) Top view of specimen 12114.76 with finger-like and globular projections. Scale bars: 5 mm.
Figure 4 Sectioned specimens of Endostoma sp. aff. nodosa MOZ-Pi 12114. (a) Polished longitudinal section, showing the axial canal. (b) Lateral view of the weathered surface, showing the non-spicular skeleton. (c) Detail of rectangle in (b). (d) Polished section showing details of the skeleton. (e) Detail of rectangle in (d), arrows point to scattered triactine spicules. (f) Transversal polished section of a tube, showing the axial canal. (g) Polished section showing the arrangement of the fibres. (h) Lateral view displaying the system of inhalant pores showing a triactine arrangement.
Description: Small specimens are either club shaped, globular or sub-cylindrical; branching specimens are sub-cylindrical (Fig. 3). Most fragments are longer than wide. Mean preserved length is 24.02 mm (minimum = 11.52; maximum = 44.47). Mean preserved width is 16.93 (minimum = 8.69; maximum = 48.62). Rounded osculum, of 1–2 mm in diameter, at the top. Most specimens are isolated, but some are tubes conjoined by their bases, or bundles of short tubes starting from a common base (Fig. 3a, e–g). Some specimens retain the dermal layer, but in most of them it is slightly weathered or recrystallised, showing the reticulated arrangement of the non-spicular skeleton, made of fibres which show a very fine lamellar structure. Some scattered triactine spicules can be observed. Slightly weathered surface pores are formed by bundled triactine spicules. An axial canal, of about the same diameter as the osculum, extends from it to almost the base of the sponges (Fig. 4a). EDS analysis showed two distinct peaks corresponding to calcium carbonate and silica – when targeting the matrix the maximum peak is on calcium, while in the skeleton the main peak is on silicon.
Occurrence. AF, Hoplitocrioceras gentilii Zone, Lower Hauterivian, Cerro Marucho, Neuquén Province, Argentina.
Discussion: ‘Corynella’ nodosa was described by Keeping (Reference Keeping1883) as a more or less pyramidal to rarely cylindrical species, attached by a broad base; sessile, or mounted upon a short neck. Sponge walls are very thick, composed of a uniform, coarse vermiculate tissue, leaving only a narrow cylindrical central cloaca. A system of lateral canals opens into the central cloaca but is imperfectly developed. Osculum terminal, central. A simple smooth area forms the terminal cone around the osculum, but below this the surface is raised into prominent, coarse knobs and foldings. No measurements were given, but specimens depicted on the Sedgwick Museum's website (http://www.sedgwickmuseum.org/index.php?page=collections) where the materials are deposited allowed some size estimations (diameter less than 1 cm); Keeping's paratypes, specimens SM 26242, 26244, 26245 and 26248 (repository numbers) can be assigned to this species. Unfortunately, the holotype is not figured.
Hurcewicz (Reference Hurcewicz1975, p. 237) described specimens assigned to ‘Corynella’ nodosa as follows: ‘solitary, subcylindrical, slender, gradually thinning out to the form of a short hypophare ended with small projections. Wall surface equal, without cortex, with transversal growth rings. Osculum 1.75–2.10 mm in diameter, with rounded margins, situated in depression.’. Hurcewicz (Reference Hurcewicz1975) illustrated specimens that are more elongated than those of Keeping (Reference Keeping1883), and they closely resemble the materials studied here. On the basis of all characters shared by our materials and those described by other authors, we assign these sponges to Endostoma aff. nodosa. An open nomenclature treatment is preferred due to geographical and temporal distance between previous records and ours.
The specimens studied herein can be easily differentiated from E. bullata (Étallon Reference Étallon1860), E. clava (Opplinger 1929), E. costata (Stahl Reference Stahl1824), E. intermedia (Münster Reference Münster and Goldfuss1829), E. langtonensis (Hinde Reference Hinde1893), E. madreporata (Quenstedt Reference Quenstedt1879-78), E. parva (Étallon Reference Étallon1859), E. perplexa (Quenstedt Reference Quenstedt1879-78), E. polonica (Hurcewicz Reference Hurcewicz1975), E. quendstedti (Zittel Reference Zittel1880), E. stellata Senowbari-Daryan et al. Reference Senowbari-Daryan, Fürsich and Rashidi2020 and E. stolata (Zittel Reference Zittel1878) on the basis of differences in size and shape. Endostoma cribrata (Hinde Reference Hinde1893) resembles the specimens studied here in some respects but differs from them in having larger osculi and forming colonies of lower relief and smooth outer walls.
Two of our specimens (numbers MOZ-Pi 12114.20 and 12114.106) have slightly wider diameters (14 mm) and slightly bigger osculi (3 mm) than the rest, thus resembling E. divisa (Müller Reference Müller1984), from the Tithonian of Germany; but one of them (MOZ-Pi 12114.106) is part of a bundle of short tubes with a common base, the others being noticeably smaller, so we interpret that those measurements remain within the natural variability of the species.
4. Sponge sclerobiont community analysis
Considering all 137 specimens, only 11 bore no sclerobionts, thus 91.97% of sponges were encrusted by at least one sclerobiont. Overall minimum (see below) sclerobiont richness is nine, comprising exogyrid oysters, cyclostome bryozoans, sabellid and serpulid polychaetes and agglutinating foraminifers (Figs 5, 6). Some serpulids were undetermined as their preservation prevented generic identification; these specimens are preserved as ‘half-tubes’, because their upper halves have been naturally eroded or dissolved away (Fig. 5d, e); these were not included in the richness metric, since they could either correspond to the already identified serpulid taxa, or else, correspond to entirely different taxa. Thus, the measured richness is considered as a minimum value.
Figure 5 Sclerobiont fauna in Endostoma sp. aff. nodosa MOZ-Pi 12114. (a) Lateral view of specimen 12114.8, showing lateral buds and abundant inhalant openings. Towards the lower end, a partially bioimmured left oyster valve can be distinguished. (b) Specimen 12114.14 in lateral view, showing encrusting bryozoans and an irregular transversal mark (see detail in Fig. 6). (c) Specimen 12114.17 with a large serpulid (Propomatoceros) partially overgrown by two bryozoan taxa (see detail in Fig. 6). (d) Small branch fragment (specimen 12114.62) showing the ‘half-tube’ serpulid preservation and a marking of irregular shape. (e) Lateral view of specimen 12114.81 showing a large oyster left valve encrusted by small serpulids preserved as half-tubes. (f) Upper view of specimen 12114.80 showing bioimmured oyster by the osculum. (g) Lateral view of specimen 12114.64, encrusted by agglutinated foraminfers. (h) Lateral view of specimen 12114.33 showing partially bioimmured oyster left valve. (i) Lateral view of specimen 12114.82 showing an irregular mark. (j) Small, branched specimen (number 12114.91) with a tricarinate serpulid growing at the base of the branch. Black arrowheads point to partially bioimmured left oyster valves; grey arrowheads indicate markings on the sponge skeleton. Abbreviations: Bry = bryozoans; Foram. = foraminifers; LS = large serpulid (genus Propomatoceros); OLV = disarticulated, cemented oyster left valve; SHT = serpulid ‘half-tube’ preservation; TCS = tricarinate serpulid (genus Mucroserpula). Scale bar: 5 mm.
Figure 6. Scanning electron microscope pictures of sclerobionts in Endostoma sp. aff. nodosa MOZ-Pi 12114. (a) ‘Berenicea’ sp. to the right, partially overgrowing foraminifers. Specimen 12114.22. (b, d) Detail of agglutinating foraminifers (both in specimen 12114.22). (c) Detail of specimen 12114.17 (see Fig. 5) showing encrusting Propomatoceros partially overgrown by Idmonea? sp. (e) Detail of specimen 12114.14, showing encrusting ‘Berenicea’ and detail of the mark on the sponge and bryozoan skeleton. (f) Detail of a Neuquenopora colony in specimen 12114.22. See Table 1 for sclerobiont identification. Scale bars: 500 μm.
Table 1 Presence–absence data of sclerobiont on sponges.
‘# sponges’ represents the number of sponges bearing at least one individual of a given sclerobiont taxon. ‘% sponges’ lists the percentage of sponges (over the total) that corresponds to the previous figures.
Table 1 lists the general metrics on presence–absence data for sponges. Oysters were the most widespread across sponges, followed by undetermined serpulids and foraminifers. Two bryozoan taxa and one serpulid taxon were also quite common on sponges, with the remaining sclerobiont taxa being found in less than 10% of sponge specimens (Fig. 7a). Minimum richness per sponge specimen is one sclerobiont taxon, and maximum richness is seven sclerobiont taxa (mean is 2.53 taxa per sponge specimen; Figure 7b). Figure 7c represents richness of sclerobionts per sponge, distributed according to the size of the latter. It shows that while larger sponge fragments host a larger number of sclerobiont taxa, smaller sponges can also quite commonly do so too. Considering that most specimens are actually sponge fragments, richness per sponge specimen may have been higher.
Figure 7. Statistical results of the sclerobiont fauna on Endostoma sp. aff. E. nodosa. (a) Bar plot showing the number of sponges bearing at least one specimen of a given sclerobiont taxon. Taxon names are shortened to their first four letters; see Table 1 for full names. (b) Bar plot showing the number of sponges with a given value of sclerobiont richness. (c) Plot of maximum width versus maximum height of sponges. Dot size represents richness of sclerobionts in each sponge. Green dots represent complete sponge specimens. Abbreviations: A.F. = agglutinated foraminifers; U.S. = undetermined serpulids.
Interactions were common among sclerobionts. Table 2 lists the 19 pairs of interactions recorded on the sponges, with a total of 34 occurrences. Here it must be remarked that some of them may be considered as possibly redundant, as they involve undetermined serpulids and thus may be the same serpulid taxa represented among well-preserved tubes. Correcting for these possible redundancies, 17 pairs of interaction were recorded among sclerobionts. They cannot be unequivocally regarded as in vivo interactions because no skeletal modification is evident in any of the participants; in addition, many interactions took place over disarticulated left oyster valves, or involved overgrowth of serpulid tubes by bryozoans, but away from the tube's aperture. Some overgrowths involve up to four different taxa settling upon each other. In many cases, large serpulids were almost completely covered by the cyclostome bryozoan Idmonea? sp.
Table 2 Interaction pairs among sclerobiont taxa.
The taxon to the left represents the overgrowing organism; to the right the overgrown taxon. Occurrences represents the number of times each interaction was observed.
The most common interactions consist of (clearly post mortem) overgrowth of disarticulated left-oyster valves by cyclostome bryozoans (Table 2). Interactions show that no sclerobiont taxon consistently overgrew others. Individual frequencies of occurrence of each interaction pair are low; only for seven pairs was more than one occurrence recorded, and the maximum occurrence for a single pair is five. All interactions for which more than one occurrence was recorded involve bryozoans overgrowing serpulids, oysters, foraminifers and other bryozoans, and foraminifers overgrowing the cyclostome Idmonea? sp. The pair Idmonea?–‘Berenicea’ overgrew each other with an almost equal amount of occurrences, and no skeletal modifications were recorded on their zoaria that can prove without question that this happened in vivo.
Interactions were also recorded between the basibiont sponges and oysters; 53 sponge specimens presented one or more oyster valves that had been partially bioclaustrated by the sponge skeleton (Fig. 5a, f, h). They represent 38.69% of the total amount of sponge specimens and 51.96% of sponges bearing oyster sclerobionts. Thus, oyster bioclaustration was a quite common occurrence; furthermore, this is a minimum estimate as more oyster valves may have suffered complete bioclaustration and are thus undetectable unless a section of the sponge specimen is made. These bioclaustrated oysters consist in left valves only.
In addition, 20 sponge fragments presented markings on their skeletons. They represent varied morphologies (Fig. 5b, d, i), the margins of which are frequently distinct. They are placed in the middle part of the branches rather than in their upper ends.
Finally, some trends were observed occasionally in a few sclerobiont taxa, regarding their orientation and/ or placing with respect to the sponge's skeleton. Oysters are commonly found in the immediate proximity of the osculum. Some of these were actually bioclaustrated by the sponge. Occasionally, bryozoans were also growing in the immediate proximity of the osculum. Serpulids are sometimes aligned to the sponge's growth axis, and in a few sponges, large serpulid tubes formed a loop that made at least a whole turn around a sponge's branch. Other serpulids grew below an expanded fold or crest of the sponge.
5. Discussion
5.1. Comparison of Endostoma sp. sclerobiont community with other study cases from the AF and interpretation of the sclerobiont community
Endostoma sp. is by far the smallest basibiont studied so far from the AF. Substrate size can impact the richness of a sclerobiont fauna (e.g., Osman Reference Osman1977; Keough Reference Keough1984; Alexander & Scharpf Reference Alexander and Scharpf1990), but richness in Endostoma sp. is comparable to that of much larger molluscs (see Table 3), especially as it is a minimum value given the incomplete preservation of most serpulid tubes. In addition, the sclerobiont community in these sponges is taxonomically very similar to that of molluscs: all taxa found in Endostoma sp. are common sclerobionts in various other invertebrate shells, reinforcing the hypothesis that these sclerobiont taxa were quite capable of settling upon very different basibionts, corresponding also to varying settings. In addition, oysters are also always the most common sclerobiont taxon, which has been attributed to its persistent high abundance in the Neuquén Sea and their pioneer role in the exploitation of organic hard substrates (Toscano et al. Reference Toscano, Lazo and Luci2018; Luci et al. Reference Luci, Toscano and Lazo2019).
Table 3 Comparison of Endostoma sp. aff. nodosa sclerobiont fauna with those of several molluscs from the Pilmatué Member.
For further details on these, see 1Luci & Cichowolski (Reference Luci and Cichowolski2014); 2Luci & Lazo (Reference Luci and Lazo2015), 3,4Luci et al. (Reference Luci, Cichowolski and Aguirre-Urreta2016, Reference Luci, Toscano and Lazo2019).
A feature observed in Endostoma sp. that is not common among mollusc basibionts and their sclerobiont communities is the presence of four bryozoan taxa. In most molluscs, only the ubiquitous ‘Berenicea’ is found. The exception is the large epifaunal pectinid Prohinnites, in which four cyclostome taxa were recorded. Prohinnites, also from the Pilmatué Member of the AF, is abundant only in the Picún Leufú depocentre of the Neuquén Basin (though scarce, fragmentary records may be found in the Mendoza sector of the basin, and even more rarely in central Neuquén; see Fig. 1), as is Endostoma sp. It has been suggested that the more calcareous nature of the sedimentation in this area of the basin may have been better tolerated by bryozoans than the mixed carbonate–siliciclastic sedimentary input typical of the central part of the basin (see Luci & Lazo Reference Luci and Lazo2015). The recording of the same trend in a second study lends further support to this hypothesis. Both basibionts also have the highest number of interaction pairs among sclerobiont taxa and the highest number of sclerobiont–sclerobiont interaction occurrences. Both were also the most commonly encrusted, with over 90% of specimens having at least one sclerobiont.
However, Prohinnites valves were large and thick, offering stable settlement substrates, while Endostoma sp. only reached a few centimetres high and offered a much smaller surface for attachment. Thus, Prohinnites was commonly and extensively encrusted because it offered a long-lasting, stable substrate. In contrast, the common colonisation of small Endostoma sp. by sclerobionts may be reflecting a lack of other available substrates in the immediate area; in contrast, Prohinnites was accompanied by abundant benthic fauna, so even though it was an attractive option for settlement, it was not the only one. In addition, the upwards growth direction of Endostoma sp. was taken advantage of by several sclerobionts, such as serpulids that commonly grew along the sponge vertical axis; this is also suggestive of in vivo settlement of some serpulids at least. Also, serpulids growing in this manner could also have been taking advantage of the sponge's exhalant flows. Vertical growth is an advantageous factor for sclerobionts that bivalves can rarely provide. The irregular morphology of the sponge, with its crests and ridges, also provided a somewhat more sheltered habitat in its undersurfaces, that were taken advantage of by foraminifers and small serpulids. The scarcity of other substrates for settlement is likely the reason why overgrowths among sclerobionts, even if post mortem, are much more common in Endostoma sp. than in molluscs, even those located in shallower, more densely populated settings such as Prohinnites, and also than those that endured a much more prolonged time of exposure, such as the cephalopods.
Few studies have reported the presence of sclerobionts on fossil sponges, and most of these examples deal with Palaeozoic occurrences (see Gundrum Reference Gundrum1979; Carrera Reference Carrera2000 for a short summary). Apart from calcareous tubes of uncertain affinity, other common Palaeozoic sclerobionts on sponges included bryozoans, brachiopods, acrothoracic barnacles, tabulate and rugose corals, pelmatozoans, foraminifers and other sponges (Gundrum Reference Gundrum1979; Palmer & Fürsich Reference Palmer and Fürsich1981; Carrera Reference Carrera2000; Taylor & Wilson Reference Taylor and Wilson2003). Mesozoic sclerobionts on sponges include bivalves, serpulids, brachiopods, sponges, bryozoans, corals, foraminifers, algal and microbial crusts (Palmer & Fürsich Reference Palmer and Fürsich1981; Fürsich & Werner Reference Fürsich and Werner1991; Leinfelder Reference Leinfelder1992). Thus, the sclerobionts found in Endostoma sp. from the Neuquén Basin are, in taxonomic terms, in agreement with the known sclerobionts on sponges from the fossil record. This sclerobiont community is rather typical of other known Cretaceous examples (see Taylor & Wilson Reference Taylor and Wilson2003 and references there, for an overview). The oldest known bioimmuration (Taylor Reference Taylor1990) is from the Ordovician of the United States, and involves the preservation of several soft-bodied and hard-bodied invertebrates on the underside of bryozoans. There are not many examples of bioimmuration of invertebrates by sponges (but see Carrera Reference Carrera2000; Cónsole-Gonella & Marquillas Reference Cónsole-Gonella and Marquillas2014), so this could be the oldest known record of bioclaustration by sponges.
The term bioclaustration (Taylor Reference Taylor1990) has been used in a flexible way here (see section 4), since though it refers to the complete overgrowth of a soft-bodied organism by the skeleton of another, preserving its shape as a hollow mould, the process is very similar to the case of complete encasing of the skeleton (or part of it) of an organism by that of another. The common presence of bioclaustrated oysters indicates that in vivo settlement of sclerobionts was common, at least in the case of oysters, and that they were not harmful for the sponge. It is likely that sponges were not strongly affected by sclerobiont settlement due to the numerous inhalant openings in their skeleton. In fact, the finding of oysters as the sole preserved settlement substrates for sponges strongly suggests that in Cerro Marucho these two species established a positive feedback loop between them, in which they served as settlement substrate for each other in soft-bottom settings in which other invertebrate taxa were apparently incapable of inhabiting. Moreover, oysters sometimes seem to have taken advantage of the exhaling currents of Endostoma sp., as suggested by the common bioclaustration of oyster valves next to the osculum. Thus, oysters not only took advantage of the skeletons of the sponges for settlement, but also occasionally established a commensal relationship with them. This likely had little effect on Endostoma sp., as the filtering process performed by the sponge remained mostly unaltered, except for the covering of some inhalant openings. But, as stated above, the latter were very numerous, and eventually, following the oyster's death and disarticulation, the sponge managed to engulf the left oyster valves, which were the largest sclerobionts and thus the ones that covered the most pores. By overgrowing them, the sponge eventually recovered the inhalant surface covered by the oyster's left valves. It is curious that no other sclerobionts have been found at least partially bioclaustrated by the sponges. Serpulids, sabellids and foraminifers were perhaps ignored by the sponge due to their tubes covering smaller areas than oyster valves, and thus clogging fewer inhalant openings at a given section of the sponge skeleton. Though large serpulids may, as a whole, have covered more openings than small oysters, these clogged inhalant openings are distributed across the sponge branch, while those covered by oysters are concentrated on their settlement spot. Bryozoans did occasionally cover quite a large area on sponges but seem to have remained undisturbed. These cyclostome taxa show no defensive structures, so it is unlikely that they defended themselves against the sponge. It is possible that the sponge was capable of overgrowing dead sclerobionts only, thus left oyster valves were the most common bioclaustrated ones.
The markings on the sponge's skeletons are difficult to interpret. Though some of them have morphologies that suggest manipulation by possible predators, or at least breakage (Fig. 5b, i), these morphologies are highly irregular and differ among specimens; not two markings are alike. Possible predators recorded elsewhere in the Hoplitocrioceras gentilii Zone of the AF include lobsters (Aguirre-Urreta Reference Aguirre Urreta1989; Andrada et al. Reference Andrada, Lazo, Bressan and Aguirre-Urreta2022). Durophagous fishes have also been recorded in the AF (e.g., Bocchino Reference Bocchino1977; Gouiric-Cavalli et al. Reference Gouiric-Cavalli, Remírez and Kriwet2019). Thus, possible predators are known to have dwelt in the Neuquén Basin during the accumulation of the AF, but it is still difficult to confirm any of them as predators for the sponges.
Some other markings, however, are not suggestive of breakage (Fig. 5d), but represent small areas of the sponge skeleton where growth was apparently temporarily interrupted. At least some of these markings may correspond to the sponges encountering other sponges or their sclerobionts and growing around these foreign objects, resulting in their partial bioclaustration. Another possibility is that soft-bodied sclerobionts had established themselves at these sites but were subsequently overgrown by the sponges. This is an interesting possibility as it is highly unlikely that the presence of soft-bodied sclerobionts would be recorded on mollusc shells, but the capability of the sponges to overgrow these sclerobionts could allow these soft-bodied organisms to be recorded as traces. However, with the data available up to now no further inferences can be made in order to confidently settle the matter. Thus, the issue of their origin remains open.
5.2. Life history of the sponge meadow
The sponge meadow reported here is of special interest for comparison with the previously described benthic communities of the AF as it represents the maximum development and abundance of sponges in the unit. Sponges, very similar to the ones described here but much smaller in size, have been recorded attached to ramose coral colonies in a few stratigraphic levels of the AF (Lazo et al. Reference Lazo, Cichowolski, Rodríguez, Aguirre-Urreta, Veiga, Spalletti, Howell and Schwarz2005; Garberoglio Reference Garberoglio2019). So, even as sclerobionts, sponges are rare in the unit, because corals appear only at discrete levels scattered across the AF, comprising either coral meadows or patch-reefs. The situation of Mesozoic sponge meadows outside the Neuquén Basin will be considered further in the Discussion, Section 5.3. But within the AF, sponges are absent from benthic communities except for this meadow and their presence as sclerobionts on corals.
The sponge meadow is restricted stratigraphically and geographically. It is recorded only in the locality of Cerro Marucho, despite the surveying efforts carried out in several nearby localities where the same levels are exposed (see for example localities in Cataldo & Lazo Reference Cataldo and Lazo2012; Luci & Lazo Reference Luci and Lazo2015). Its lenticular shape and limited vertical development, together with the small size of the sponges, suggests that the conditions for their settlement were quite limited in space and time.
The history of the sponge meadow can be reconstructed as follows. In a soft-bottom setting within the outer ramp, oysters were the only benthic dwellers locally at this particular time within the H. gentilii Zone. Benthic fauna were already scarce, as below the sponge meadow only an oyster shell bed is recorded. Ceratostreon oysters had a facultative reclining life habit which in addition to their small size and thin shells would have prevented them from sinking in the soft, muddy bottoms, allowing early colonisation. Oyster mass occurrences are not rare in the Early Cretaceous AF and are often formed in outer ramp settings (Toscano & Lazo Reference Toscano and Lazo2020). In some cases, they have been associated with increased nutrient input conditions and/or relatively increased sedimentation rates (Toscano et al. Reference Toscano, Lazo and Luci2018). They may be traced almost basin-wide, and replace the usual benthic communities composed by a variety of bivalves, gastropods and to a minor extent, decapods, echinoderms and other invertebrates (see, for example, Lazo et al. Reference Lazo, Cichowolski, Rodríguez, Aguirre-Urreta, Veiga, Spalletti, Howell and Schwarz2005; Lazo Reference Lazo2007b) . Thus, conditions in this interval in the Cerro Marucho locality were already indicative of an environmental setting that did not allow the typical benthic macrofaunal association of the AF to thrive, before the sponge meadow established itself.
Sponges took advantage of abundant oyster valves to settle themselves and thrived on this otherwise soft bottom for some time (pioneer stage; Fig. 8a). Sponges were then encrusted by oysters, which in turn provided, at their death, additional valves for further sponge colonisation. Oysters were the early settlers/pioneers as sclerobionts because they were already present in the sea bottom. Oysters were then followed by sabellids, serpulids, foraminifers and bryozoans which often overgrew each other (climax stage) and were not, apparently, bioclaustrated by the sponges, probably due to their covering fewer inhalant openings (Fig. 8b, c). Sclerobionts most likely settled preferentially on sponges due to their higher elevation above the substrate than the oysters. Bryozoans occasionally covered serpulid tubes, most likely causing no harm had the serpulids still been alive, as long as openings were not obliterated. Bryozoans are often the overgrowing organisms in sclerobiont–sclerobiont interactions, but this may be because they were late settlers or because they are the only colonial organisms among sclerobionts, and thus more easily able to overgrow older, dead or inert skeletal parts of other sclerobiont taxa.
Figure 8. Succession sequence of Endostoma sp. aff. nodosa meadow. (a) Initially, within a quiet, soft bottom and probably exaerobic setting, with relatively high sedimentation rate and nutrient input, oysters were the sole organisms able to thrive. Their valves provided hard substrate (taphonomic feedback) in an otherwise sterile bottom, which was eventually exploited by Endostoma sp. aff. nodosa, giving way to the pioneer stage of the meadow. During this stage, sponges were on their early growth stages. (b) With time, sponges grew considerably and a dynamic sclerobiont community developed on them, representing the climax stage of the meadow. Oysters were early settlers, followed by sabellids, serpulids, foraminifers and bryozoans, which, in turn, often overgrew each other. (c) Detail of the sclerobiont community that developed on E. aff. nodosa. Several interactions between the sclerobionts and with the sponges were recorded (see also Table 2). (i) Serpulid overgrowing a ‘Berenicea’ sp. colony; (ii) Ceratostreon sp. left valve bioimmured by E. sp. aff. E. nodosa; (iii) serpulid overgrowing Ceratostreon sp. left valve; (iv) ‘Berenicea’ sp. colony overgrowing an agglutinating foraminifer. (d) Shortly after the climax stage, the meadow perished. An intensification in sedimentation rate and/or nutrient input beyond a threshold manageable for the sponges may have been the cause(s) of their demise.
After a fairly short time, the sponge meadow perished (Fig. 8d). Though sponges are fragmented and not preserved in life position, no evidence of storm events was recorded in the field. One possible cause for the demise of this low-relief community could be increased sedimentation. A lack of oxygen within the first centimetres of the water column would imply extraordinary palaeoenvironmental changes of which there are no indication. High rates of sedimentation coupled with an elevated nutrient input were factors already in place as suggested by the high abundance of reclining oysters at the base of the sponge-bearing bed. An intensification in either sedimentation rates or nutrient input (or both) may have been the cause(s) of the meadow's demise. Sponges have been reported to tolerate higher sedimentation rates than other benthic taxa (see section 5.3) but being filter feeding animals they are still incapable of enduring sedimentation beyond a given threshold. The optimal conditions for sponge development existed only for a short period of time, and after conditions changed, the benthic fauna did not immediately flourish, since only ammonites are found in the interval above the sponge-bearing level.
5.3. Similar Mesozoic occurrences worldwide
The Mesozoic record of Calcarea is very sparse, and more so when it concerns forms similar to Endostoma sp. as the main benthic elements constituting sponge meadows or build-ups. Most known cases are from the Jurassic of Europe, especially from the Kimmeridgian of Portugal (Fürsich & Werner Reference Fürsich and Werner1991; Leinfelder Reference Leinfelder1992; Werner et al. Reference Werner, Leinfelder, Fürsich and Krautter1994). Several Endostoma species have been mentioned as forming ‘moderately large’ communities in some ‘sheltered parts of the basin’ in the Oxfordian of Poland, as reported by Hurcewicz (Reference Hurcewicz1975). However, this paper focused on the taxonomy of sponges, and thus the author did not elaborate much further on the ecological function and environmental setting of these sponges. Also, Reitner (Reference Reitner and Wiedmann1989) mentioned sponges communities containing Endostoma from the Aptian Faringdon ‘Sponge Gravels’ of England and Aptian–Albian coralline sponge communities from Spain. The role of Endostoma was not specified.
Palmer & Fürsich (Reference Palmer and Fürsich1981) reported sponge patch reefs to bioherms with Endostoma as accessory frame builders from the Upper Bathonian of France. The environmental interpretation for these build-ups was a relatively shallow setting, below fair-weather wave-base but above storm wave-base, within the lower photic zone. Fürsich & Werner (Reference Fürsich and Werner1991) described low sponge–coral meadows from the Kimmeridgian of Portugal, in which Endostoma was a part of the frame-builder association. This association was interpreted as belonging to a shallow fully marine environment, with low sedimentation rates and moderate to low energy levels punctuated by occasional high energy events. Fürsich & Werner (Reference Fürsich and Werner1991) noted an increase in sponge abundance in detriment of corals towards the south-east, which they attributed to an increment in turbidity in that direction; sponges may have been able to cope with it better than corals. In addition, they noted that occasionally, greater influxes of fine-grained particles took place that probably prevented corals and sponges' growth.
Complex coral reefs from the Kimmeridgian of Portugal had several coralline sponges as possible accessory frame builders, including Endostoma in a high-energy setting above fair-weather wave base (Leinfelder Reference Leinfelder1992). Also, from the Kimmeridgian of Portugal and Germany, Endostoma was reported within lenticular crinoid–coral mounds, hexactinellid and other siliceous sponge meadows, in which it did not play an important role (Werner et al. Reference Werner, Leinfelder, Fürsich and Krautter1994). The inferred environmental setting was a fully marine, low-energy and low-sedimentation outer slope. Werner et al. (Reference Werner, Leinfelder, Fürsich and Krautter1994) drew a conclusion that is of relevance here: an increase of siliceous and calcareous sponges at the expense of corals could be caused by a slight increase in sedimentation, nutrients, or lowered oxygenation. Thus, sedimentation and nutrient input are reported as factors for which sponges may have increased tolerance as compared to other benthic fauna (especially other reef builders) but they may, under extreme conditions, hinder their development also.
Clearly the development of a low-relief, monospecific sponge meadow in Cerro Marucho corresponds with geographically and temporally limited, very specific conditions that allowed the sponges, a rare and marginal component of benthic faunas along the AF and other reported examples, to colonise the sea bottom as the main, and almost sole, benthic component, along with small Ceratostreon oysters. This is a previously unreported mode of occurrence of Endostoma sp. and similar sponges, the first for the Cretaceous outside the Tethyan Realm, and could draw attention upon other similar examples previously unnoticed.
6. Conclusions
This is the first record of calcareous sponges belonging to Endostoma for the Neuquén Basin and adds to the few known reports outside the Tethyan Realm. Despite usually being described as accessory builders or even accessory components of different types of build-ups, Endostoma could construct short-lived, low diversity, low relief meadows on quiet settings in association with small oysters. Sponges also housed a quite diverse sclerobiont community in an otherwise soft bottom. These sponges were quite capable of overgrowing sclerobiont oysters, which proves that at least some of the recorded encrustation took place in vivo. Some sclerobionts' growth direction and placement were also suggestive of live interaction with the basibiont sponge. Oysters and some serpulids may thus have established a commensal relationship with Endostoma. This example adds to the knowledge about the genus' palaeoecology by presenting a hitherto unknown role for small calcareous sponges.
7. Acknowledgements
Two anonymous reviewers and the Editor are thanked for their valuable contributions to this manuscript. The authors thank Dr M. Tunik for her help during fieldwork. Technician M.M. Pianetti is thanked for her invaluable help with getting and imaging the materials in the scanning electron microscope while still under partial restrictions during the world COVID-19 pandemic.
8. Financial support
Funding for this work was provided by the grant UBACyT 2018 issued to Dr D.G. Lazo. This is contribution R-424 of the Instituto de Estudios Andinos ‘Don Pablo Groeber’.
9. Competing interests
None.
