**The Cost for Biodiversity: Records of Ciliate–Nematode Epibiosis with the Description of Three New Suctorian Species**

**Elisa Baldrighi 1, Igor Dovgal 2, Daniela Zeppilli 3, Alie Abibulaeva 2, Claire Michelet 4, Emma Michaud 4, Annalisa Franzo 5, Eleonora Grassi 6, Lucia Cesaroni 6, Loretta Guidi 6, Maria Balsamo 6, Roberto Sandulli 7,\* and Federica Semprucci <sup>6</sup>**


http://zoobank.org/urn:lsid:zoobank.org:pub:D2927905-34B3-402B-AA81-0C13D12D1D81 Received: 4 May 2020; Accepted: 1 June 2020; Published: 4 June 2020

**Abstract:** Epibiosis is a common phenomenon in marine systems. In marine environments, ciliates are among the most common organisms adopting an epibiotic habitus and nematodes have been frequently reported as their basibionts. In the present study, we report several new records of peritrich and suctorian ciliates-nematode association worldwide: from a deep-sea pockmark field in the NW Madagascar margin (Indian Ocean), from a shallow vent area in the Gulf of Naples (Mediterranean, Tyrrhenian Sea), in a MPA area in the Gulf of Trieste (Mediterranean, Adriatic Sea), from a mangrove system in French Guiana (South America, Atlantic Ocean), and from the Maldivian Archipelago. In addition, three new species of Suctorea from the Secca delle Fumose shallow vent area (Gulf of Naples) were described: *Loricophrya susannae* n. sp., *Thecacineta fumosae* n. sp. and *Acinetopsis lynni* n. sp. In the light of these new records and data from the existing literature, we discuss the suctorian–nematode epibiosis relationship as a lever to biodiversity.

**Keywords:** epibiosis; ciliophora; suctorea; nematoda; meiofauna; biodiversity

#### **1. Introduction**

Epibiosis (greek *epi* "on top" and *bios* "life") is a facultative spatial association between two organisms: the epibiont and the basibiont [1]. Epibionts are organisms that, during their sessile phase, remain attached to the surface of a living substratum, while the basibiont provides the support for the epibiont. Both concepts suggest ecological functions [2,3]. Epibiosis is a common phenomenon in marine systems and can be considered a direct consequence of surface limitation and/or a wave

turbulence effect that obliges many lightweight organisms to evolve attachment systems to adhere to hard and relatively stable surfaces (e.g., of other living organisms; [4]). Epibiosis is the evolutionary result of an interaction between environmental factors and benthic life forms; it is a dynamic process and the ecological consequences for the basibiont and the colonizer (e.g., bacteria, fungi, algae and protozoans) can be of different nature (i.e., positive, negative or without effects for the host) depending on the environmental conditions and on the epibiotic assemblage composition and density [1,3,5]. Direct and indirect interactions among epibionts and with the host, and changing environmental conditions drive the dynamics of the epibiotic community [1]. Epibiosis can be temporary, i.e., linked to the seasonal presence of the basibiont and /or epibiont or it can represent a temporary colonization due to a decrease in basibiont defenses or to its fitness. Epibiosis may modify a number of interactions between the basibiont and the biotic and abiotic components of the environment [3,5,6]. This is the reason why epibiosis may act as an ecological lever by modifying and greatly amplifying or buffering biotic and abiotic stresses [5]. In some cases, epibionts are considered as commensals (e.g., [7]) because they are not harmful to the hosts; however, some of them can indirectly influence growth, survival rate and reproductive capability of basibionts, showing a negative impact on their fitness [5,8].

Epibiotic assemblages are rarely species-specific [2], and many colonizers are substratum generalists. Different basibiont species may also host different epibiotic communities (e.g., [9,10]). In most investigations, less than 20% of epibionts were reported as restricted to this mode of life, and less than 5% occur exclusively on one basibiont species [11,12]. Nevertheless, some exceptions were documented in previous studies (e.g., [7,13,14]) indicating species-specific host-epibiont relationships. In general, the epibiont must be able to cope with the basibiont lifestyle and its surface properties. The properties of the basibiont surface, i.e., its consistency, surface ornamentation, the presence of previous settlers (e.g., biofilms) and the deployment of defenses, determine which of the available potential epibionts will successfully settle and grow when a suitable substratum becomes available. Indeed, many basibionts have developed a variety of defense mechanisms to prevent epibiosis or to remove epibionts: these span from mechanical defenses (e.g., mucus secretion, burrowing behavior, movement in narrow caves for abrasion and epibiont elimination) to chemical methods (e.g., secretion of secondary metabolites such as antibacterial or antifungal compounds), if the nature of the relation is disadvantageous [3,15].

An important component of epibiont communities are ciliated protozoans. These organisms also constitute a significant component of the overall marine and freshwater ecosystems, and play an important role in the food chain [16]. Suctorian ciliates, together with peritrichs, are the most species-rich groups of Ciliophora. They live in all types of water bodies and they are epibionts on a wide diversity of hosts and substrates. Some species are ectoparasitic or endoparasitic species, but many of these ciliates are commensals of aquatic invertebrates or vertebrates [17]. Suctorian ciliates are quite selective by feeding principally on small ciliates, flagellates and amoebae that are captured by tentacles [17,18].

Many meiofaunal organisms such as Copepoda Harpacticoida, Ostracoda, Halacarida, Tanaidacea, Kinorhyncha and free-living Nematoda were found to be common basibionts for suctorian and peritrich ciliates and prevalent across estuarine to marine ecosystems [14,19–21]. However, many aspects of this relationship need to be clarified: the criteria for the host selection; adhesion mechanisms; the role of environmental variables in influencing the distribution and diversity of ciliates adhered to meiofauna, and the ecological significance of epibiont–basibiont interactions across different habitats [21,22].

Nematoda is the most abundant, ubiquitous and diverse meiofaunal marine phylum [23] and they cover a key ecological role in the ecosystem processes [24]. Thanks to their cuticle characteristics, often made by a thick and multi-layered collagenous covering, they are ideal basibionts for many suctorian ciliates (e.g., [22,25]). In particular, nematodes of the families Desmodoridae and Desmoscolecidae have found to be largely colonized due to the well-developed cuticular ornamentation that favors the adhesion of epibionts (e.g., [26]).

In a recent study based on published records, Chatterjee et al. [27] provided a checklist of suctorian epibionts on meiobenthic marine nematodes. Despite the amount of data presented from different geographical zones and types of environments, this phenomenon is still largely underestimated and the nematode-ciliate association might be more common than it actually appears to be. This is mainly due to three reasons: (i) in papers concerning nematode taxonomy and/or ecology the presence of epibionts was often overlooked or simply reported without a description of the ciliate(s), their number and distribution on the basibiont body surface; (ii) the methodology used for nematode extraction from the sediment (i.e., centrifugation) may induce the loss of some epibionts; (iii) specialists of ciliate or nematode taxonomy work separately and their focus of research is usually on the taxonomy and ecology of only one of the two groups. All these aspects have largely hampered a clear comprehension of this phenomenon.

In the present paper, we reported some new finds of Suctorea from the Secca delle Fumose shallow vent area (Naples, Italy) and we described three new species. Secca delle Fumose belongs to the degassing structure offshore of the Campi Flegrei caldera and its biology and ecology has been investigated only recently [28,29]. We reported also several new records of peritrich and suctorian ciliates-nematode association worldwide, providing an update of the check-list presented by Chatterjee et al. [27]. In the light of these new records and the literature data, we discussed the suctorian–nematode epibiosis relationship as a lever to biodiversity.
