A rugose coral – bryozoan association from the Lower Devonian of NW Spain
Introduction
Intergrowth of living species is frequently developed among recent sessile organisms in environments such as reefs, where it may involve some benefit for the intergrown species in competition for a suitable substrate or in preventing predation (Ramsby et al., 2012; Wilcox et al., 2002). This has been described mainly in shadowed rocky grounds (e.g. Harmelin, 1990; Ristedt and Schuhmacher, 1985). Similar cases of intergrowth were also common in the past (Kershaw, 1987), but their occurrence in the fossil record is very difficult to assess, as functional, histological and molecular interactions such as those reported in living symbiotic organisms (Piraino et al., 1992; Van Syoc and Newman, 2010; Tsubaki and Kato, 2014; Pantos and Hoegh-Guldberg, 2011; Wilcox et al., 2002; Bondarev et al., 2013), cannot be observed. Moreover, soft-bodied invertebrates, which have a low potential for fossilisation, are known to participate in a large range of intergrowths (Montano et al., 2014; Seveso et al., 2015). Associations of skeletonized organisms are not free of uncertainties, either. In vivo association can be readily demonstrated in living specimens, but the study of fossil symbiotic associations is supported by scarce data and is unavoidably subject to limitations, as it relies exclusively on the interpretation of skeletal features and indirect evidence (Tapanila, 2008). Evidence that suggests that the components of a presumed symbiotic intergrowth were simultaneously alive can be elusive even for experienced researchers. Despite the obvious difficulties of studying fossil symbiotic associations, bioclaustration structures have allowed the descriptions of several such cases among Palaeozoic and post-Palaeozoic marine invertebrates.
Post-Palaeozoic bryozoans have been reported as hosts to corals (Cadée and McKinney, 1994; Taylor, 2015) or bioclaustrated symbionts with unknown affinities (Taylor and Voigt, 2006). There is abundant literature regarding the common existence of symbiotic relations between some recent hydroids and a few species of encrusting bryozoan hosts and these associations usually show high specificity (Boero et al., 2000; Gautier, 1962; Hastings, 1930, Hastings, 1945; Ristedt and Schuhmacher, 1985). An example of a recent symbiosis between bacteria and bryozoans producing bryostatins has been the subject of numerous projects of medical interest due to the application of these metabolites to fight illnesses such as cancer and Alzheimer's disease (Miller et al., 2016).
For decades, the vast majority of cases of Palaeozoic symbiotic associations have been described in corals and stromatoporoids (Soto and Méndez Bedia, 1985; Tapanila, 2002, Tapanila, 2005, Tapanila, 2006; Vinn, 2016a, Vinn, 2016b). Palmer and Wilson (1988) described the ichnogenus Catellocaula to name the cavities produced by growth of an Ordovician bryozoan colony around a soft-bodied symbiont. Catellocaula was the only reported case of a Palaeozoic bryozoan that hosted a bioclaustrated symbiont until Suárez Andrés (1999) reinterpreted the Devonian genus Speotrypa as a case of bioclaustration in fenestrate bryozoans, which McKinney (2009) described as the new ichnogenus Caupokeras. Recently, increased interest has led to the publication of new cases of bioclaustration in Palaeozoic bryozoans, mostly from the Lower Palaeozoic succession of Estonia (Vinn, 2016a; Vinn and Wilson, 2015, Vinn and Wilson, 2016; Vinn et al., 2014; Vinn et al., 2016; Vinn et al., 2019) but also from the Devonian of Germany (Ernst et al., 2014) and Spain (Suárez Andrés, 2014). Symbiotic relationships between worms and solitary rugose corals in North American Late Ordovician (Elias, 1985) have been reported as ‘opportunistic’ worms attached to the side of polyps in rare instances. Elias (1985) explained how these worms bored through septa within the calices and came into contact with the basal surfaces of the polyps, which secreted skeletal material that sealed off the intruders. Also in the Palaeozoic and Cretaceous there are symbiosis among three different organisms such as the one described by Morris et al. (1991) from the Devonian of New York involving a gastropod with a trepostome bryozoan and a possibly a sipunculan worm, and the one reported by Zágoršek et al. (2009) with hydroids, worms and bryozoans from the Cretaceous of the Czech Republic. Bryozoan epibiosis on fossil crabs has been described in the Miocene of Iran (Key Jr. et al., 2017).
Although bryozoans are a common component of Palaeozoic benthic faunas, reported cases of symbioses within this group are scarce when compared with those of corals and stromatoporoids. Palaeozoic bryozoan colonies are known to have interacted both with soft-bodied symbionts and modular organisms with mineralized skeletons. Embedment of soft-bodied organisms by the host bryozoans led to bioclaustration structures that allow for the recognition and interpretation of such associations (Palmer and Wilson, 1988; McKinney, 2009; Suárez Andrés, 2014; Ernst et al., 2014). On the other hand, there are overgrowths such as a bryozoan around the tabulate coral Aulopora from the Devonian of Altai in Russia (Nekhoroshev, 1948) or intergrowths like those of McKinney et al. (1990), who described the association between the same tabulate coral and the bryozoan Leioclema from the Devonian of Kentucky that is now the only reported case of intergrowth between a Devonian bryozoan and a skeletonized organism. In case of syn-vivo associations between bryozoans and non-cnidarians there are many examples in the literature, such as between bryozoans and possible polychaetes (Wyse Jackson and Key Jr., 2007). Historically, some associations were confused with anatomical structures (Spjeldnaes, 1985) such as brood-chambers or gonozooecia, giving the associated organisms a false taxonomic importance in the Ordovician.
While intergrowth between cystoporates and rugose corals was earlier described from the Late Ordovician of Estonia (Vinn et al., 2018), recent sampling of the Aguión Formation (Emsian, Lower Devonian) allowed for first time identification of specimens of fistuliporid bryozoans that hosted living rugose corals. The purpose of this paper is to describe and interpret this association, as well as compare it to similar cases, as no recent occurrences are known, between bryozoans and cnidarians from different geographical regions and stratigraphic positions.
Section snippets
Geological setting
The north of the Iberian Peninsula has scattered outcrops with Devonian strata, mostly in the Westasturian-Leonese Basin, that belongs to the Ibero-Armorican Trough (Carls, 1988). The studied fauna comes from the Upper Emsian, Early Devonian, of the Arnao Platform, at Cape La Vela (Asturias, NW Spain) (Fig. 1). The closest village to the site is Arnao, on the northern side of the Cantabrian Mountains. In this area the Lower Devonian (Upper Emsian) succession crops out showing a rich benthic
Materials and methods
We found 12 samples with intergrowth between cystoporate bryozoans and rugose corals, but only nine are clear enough to be described here. Three specimens belong to the collections of the Museum of Geology, University of Oviedo. The rest were collected in the Early Devonian of Arnao Platform (Asturias, NW Spain) by JLSA during 2017 under permits of regional and national authorities. This material is housed in the palaeontological collections of the Museo de la Mina de Arnao (Arnao Mine Museum).
Description
There are nine samples displaying very clear intergrowth between fistuliporid bryozoans and rugose corals. All of them show the bryozoan skeleton clearly distinguished from the symbiont. The colonies are from 14.2 to 25 mm long (DGO12902 and MMAGE0036 respectively) and from 12.1 to 20 mm wide (MMA4 and MMAGE0036 respectively) and about 20 mm in height. All of these samples display between one and two distinctive corallites (see Table 1 for measurements), except for DGO12903, which hosted nine
Other cases of intergrowths between bryozoans and cnidarians
Other similar cases of bryozoans developing intergrowths with symbionts with mineralized skeleton as cnidarians are those reported from the Late Ordovician of Estonia by Vinn et al., 2016, Vinn et al., 2017b, Vinn et al., 2018; Ohio-Indiana Platform by Elias (1982); and Missouri by MacAuley and Elias (1990); in the Early Devonian of Tennessee by McKinney et al. (1990); and in the Middle Devonian of New York State by Boardman (1960). In the Neogene of Europe, Cadée and McKinney (1994) and Taylor
Conclusions
The intergrowth described was facultative for the bryozoans and probably mutualistic for both partners; symbiotic rugose corals have not been observed in the fauna isolated from their hosts. The bryozoans would benefit at least from a free substrate providing access to higher tiers, and doubtless from chemical defenses which would deter predators and settlers. The corals benefited from a hard, more stable substrate that allowed for the settlement of larvae and growth without being smothered in
Acknowledgements
We thank to Andreas May (Unna Germany), Stefan Schröder (Institut für Geologie und Mineralogie der Universität zu Köln, Germany) and Blazej Berkowski (Adam Mickiewicz University, Poland) for their comments regarding the symbiotic rugose corals, Kevin Webb, NHM science photographer for most of the photographs illustrated in this paper, Marcus Key and Andrej Erns for their careful reviews, and Iván Muñiz (Arnao Mine Museum and Cultural Heritage of Castrillón Council) for curation provided of the
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