Diversity and Distribution of Peritrich Ciliates on the Snail Physa Acuta

Zoological Studies 57: 42 (2018) doi:10.6620/ZS.2018.57-42 Open Access Diversity and Distribution of Peritrich Ciliates on the Snail Physa acuta Draparnaud, 1805 (Gastropoda: Physidae) in a Eutrophic Lotic System Bianca Sartini1, Roberto Marchesini1, Sthefane D´ávila2, Marta D’Agosto1, and Roberto Júnio Pedroso Dias1,* 1Laboratório de Protozoologia, Programa de Pós-graduação em Ciências Biológicas (Zoologia), ICB, Universidade Federal de Juiz de Fora, Juiz de Fora, Minas Gerais, 36036-900, Brazil 2Museu de Malacologia Prof. Maury Pinto de Oliveira, ICB, Universidade Federal de Juiz de Fora, Minas Gerais, 36036-900, Brazil (Received 9 September 2017; Accepted 26 July 2018; Published 17 October 2018; Communicated by Benny K.K. Chan) Citation: Sartini B, Marchesini R, D´ávila S, D’Agosto M, Dias RJP. 2018. Diversity and distribution of peritrich ciliates on the snail Physa acuta Draparnaud, 1805 (Gastropoda: Physidae) in a eutrophic lotic system. Zool Stud 57:42. doi:10.6620/ZS.2018-57-42. Bianca Sartini, Roberto Marchesini, Sthefane D´ávila, Marta D’Agosto, and Roberto Júnio Pedroso Dias (2018) Freshwater gastropods represent good models for the investigation of epibiotic relationships because their shells act as hard substrates, offering a range of microhabitats that peritrich ciliates can occupy. In the present study we analyzed the community composition and structure of peritrich epibionts on the basibiont freshwater gastropod Physa acuta. We also investigated the spatial distribution of these ciliates on the shells of the basibionts, assuming the premise that the shell is a topologically complex substrate. Among the 140 analyzed snails, 60.7% were colonized by peritrichs. We observed seven peritrich species: Epistylis plicatilis and Epistylis sp. (Epistylididae); Opercularia articulata (Operculariidae); Carchesium polypinum, Vorticella campanula and Vorticella sp. (Vorticellidae) and Thuricola kellicottiana (Vaginicollidae). We observed a high prevalence of epibiosis (> 60%) when all species of ciliates were considered conjunctly. However, the prevalence was low (1-58%) when each species was considered separately, reflecting their aggregate distribution pattern. The most prevalent species were Epistylis sp. (58.60%), Vorticella sp. (14.30%) and O. articulata (13.60%). Although the epibionts were distributed through the shell’s entire extension, we observed greater values of abundance, density, diversity and dominance on the dorsal surface. Only Epistylis sp. was widely distributed on the ventral surface. We also observed that the peritrichs predominantly occupied the areas of the shell delimited by the sutures. We interpreted these distribution patterns considering that the peritrichs select their attachment sites under pressures related to basibiont behavior, physical forces that may dislocate them and protective characteristics of the shell’s areas. Key words: Brazil, Peritrichia, Physa acuta, Protozoan epibionts, Site preference. BACKGROUND at the community and the microenvironment levels (Fernandez-Leborans and Cárdenas Epibiosis is a facultative association, 2009). Epibiosis involving ciliates is relatively well widespread in aquatic environments, which documented in a number of studies addressing the involves the epibionts, organisms that remain composition of epibiotic communities (Fernandez- attached to the surface of living substrates, the Leborans and Tato-Porto 2000; Chatterjee et basibionts, during the sessile phase of their life al. 2013; Bielecka and Boehnke 2014), spatial cycles (Wahl 1989). Epibiosis not only affects the and temporal distribution of epibionts in marine organisms involved, but also promotes changes and limnetic ecosystems (Hanamura 2000; Utz *Correspondence: Tel: +55-32-21023223. E-mail: [email protected] © 2018 Academia Sinica, Taiwan 1 Zoological Studies 57: 42 (2018) page 2 of 12 and Coats 2005; Dias et al. 2008; Cabral et al. in form and ornamentation and therefore offer a 2010 2017), negative impacts on basibionts range of microhabitats that can be occupied by (Visse 2007; Souissi et al. 2013; Burris and Dam peritrich ciliates. The shell is not discarded during 2014), advantages and adaptations of epibionts the development of the snails, like it is with the (Delgery et al. 2006; Fernandez-Leborans and exoskeletons of arthropods (Hanamura 2000; Rintelen 2010), spatial colonization patterns of Delgery et al. 2006; Vicente et al. 2008), allowing epibionts on basibionts (Fernandez-Leborans et the continuous colonization by ciliate species and al. 2006; Marinõ-Perez and Mayén-Estrada 2009; leading to complex interactions between ciliate Fernandez-Leborans et al. 2013) and epibionts species in space and time (Dias et al. 2008). biology (Gilbert and Schröder 2003; Utz 2008; As a result, freshwater snails can be regarded Bickel et al. 2012). as a source of biodiversity in limnic environments Epibiont ciliates are found in several groups: (Voight and Walker 1995; Gutiérrez et al. 2003). apostomatids, chonotrichids, heterotrichs, However, most studies on the matter are restricted peritrichs and suctorians (Corliss 1979; to marine species bearing communities composed Fernandez-Leborans et al. 2006). Among these, of polychaetes and anemones (Wahl and greater diversity of epibiont ciliates are found in Sönnichsen 1992; Warner 1997; Vasconcelos et the subclass Peritrichia, Stein 1859, whose life al. 2007; Mercier et al. 2011). Studies aiming to cycles contain a sessile stage fixed by a stalk to investigate epibiotic interactions between peritrich an inert or living substrate as well as by a dispersal ciliates and freshwater gastropods are scarce, stage represented by free-swimming forms that more particularly in neotropical ecosystems seek new substrates (Gilbert and Schröder 2003). (López-Ochoterena 1964; Dias et al. 2006 2008 They can live as epibionts on several metazoans 2010; Utz 2007). as cnidarians, ctenophorans, rotifers, tardigrades, Physa acuta Draparnaud, 1805 (recent platyhelminthes, crustaceans, annelids, insect synonym Haitia acuta) (Pulmonata, Physidae) is larvae, mollusks, fishes, tadpoles and turtles (Kahl an invasive freshwater snail originating from North 1935; Corliss 1979; Foissner et al. 1992; Moss et America, presently found in all continents (Dillon al. 2001; Mayén-Estrada and Aladro-Lubel 2002; et al. 2002; Van Leeuwen et al. 2012). These Gilbert and Schröder 2003; Dias et al. 2008 2009). snails exploit several dispersal vectors that may Although the majority of peritrich species are able have contributed to its wide geographical range to colonize both inert and living substrates evenly, (Van Leeuwen et al. 2012), and there is genetic the colonization of basibionts is not a random and demographic evidence that these snails phenomenon. There is experimental evidence recurrently recolonize habitats (Bousset et al. that suggests that these ciliates actively select 2004; Chlyeh et al. 2006). They show tolerance the colonized species, as well as the attachment to a wide range of environmental conditions, sites on the basibionts (Cook et al. 1998; Mayén- including organic pollution, and were recently Estrada and Aladro-Lubel 2001; Gilbert and used as biological models to assess toxicological Schröder 2003; Fernandez-Leborans et al. 2006). effects of nanoparticles in freshwater environments The advantages of colonizing a living (Fahmy et al. 2014). They are commonly found in substrate have been mostly associated to nutrient eutrophic lakes and rivers in Europe, Asia, Africa, acquisition through the water currents generated Australia and North and South America (Paraense by the basibionts (Wahl 1989; Threlkeld 1993; and Pontier 2003; Bernot et al. 2005; Albrecht et Fernandez-Leborans et al. 2006), or from the al. 2009; Tietze and De Francesco 2010). bacteria-rich periphyton that accumulate on Herein we analyzed the community their exoskeletons (Bernot et al. 2005). Another composition and structure of peritrich epibionts important aspect is the fact that the basibionts on P. acuta. We also investigated the spatial are mobile, moving away from unfavorable distribution of these ciliates on the shells environments and thus promoting the survival of of basibionts, assuming that the shell is a the epibionts (Dias et al. 2008). Also, the basibiont topologically complex substrate. We considered may potentially promote epibiont dispersal during that the different parts of the shell represent their own migrations, contributing to the gene flow distinct microhabitats and some of its areas between populations (Wahl 1989). may be more favorable for the establishment of Freshwater gastropods are good models for epibionts. We interpreted the observed distribution investigating epibiotic relationships because their patterns, considering that the peritrichs select shells act as hard substrates that are complex their attachment sites under pressures related to © 2018 Academia Sinica, Taiwan Zoological Studies 57: 42 (2018) page 3 of 12 the basibiont behavior, physical forces that may Epibiotic community structure dislocate them and protective characteristics of the shell’s areas. To access epibiotic community structure, we analyzed the data on prevalence, mean intensity, mean abundance and the discrepancy index MATERIALS AND METHODS (Poulin 1993) for each epibiont species with the Quantitative Parasitology 3.0 software (Rosza et Snail sampling al. 2000). In all analyses, colonial peritrichs were quantified considering each zooid as an individual. We collected 140 Physa acuta specimens in

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