**1. Introduction**

Ciliates (Alveolata: Ciliophora) comprise free-living and symbiotic species. According to Corliss, [1] 2,600 species of ciliates have been described as symbionts, mainly of individuals of metazoan phyla. This is equivalent to 33% of all the known species of the phylum. They belong to eight classes (Armophorea, Heterotrichea, Litostomatea, Nassophorea, Oligohymenophorea, Plagiopylea, Phyllopharyngea and Spirotrichea), 31 orders, 151 families, and almost 700 genera [2]. These symbiotic ciliates have been reported in aerobic and anaerobic environments and from aquatic and terrestrial habitats [2, 3].

The term symbiosis can be defined as a sustained relationship between at least two individuals from different species, either living in direct contact or close enough to each other during a part or the whole life cycles of the partners. This interaction is transmitted vertically (from one generation to the next) or horizontally (acquired *de novo* in each generation). The intricate associations are believed to have an essential driving force in evolutionary biology, as a host and their symbiotic microbiota acclimatize on scales of short time [4].

Due to the diversity of symbioses, a classification system for symbiotic associations has been developed. This classification is based on several features: i) the dependence, where symbionts can be obligate or facultative; ii) specificity of the symbionts; iii) nutrients obtention, then biotrophic and necrotrophic symbionts are distinguished on the basis of whether nutrients are obtained from a living or dead partner, and iv) location of the symbionts, ectosymbionts or endosymbionts [5]. The symbiotic relationships can be categorized into mutualistic, commensalistic, or parasitic [2, 6]. The boundary between these categories sometimes is not clear, and there are frequent transitions between them.

Several papers have been focused on providing taxonomic reports for symbiotic ciliates, some of them as general works, and a few directed to certain groups [7–16], and some were focused on certain geographic areas [17–24]. Critical reviews of some species as *Balantidium coli* were done by Schuster and Ramirez-Avila [25]; for chonotrichs [26]; peritrichs [27] and suctorians [28].

Also, very different topics about ciliates and their hosts have been developed as shown: symbiotic interactions [epibiotic, hyperepibiotic, commensals, parasites (obligates and facultatives)], codiversification: [29–37]. Morphology (variation, molecular characterization): [38], clevellandellid, *Nyctotheroides*; [39], *Dicontophrya*; [40, 41] peritrichs. Taxonomy (new family, genus or species), redescription, revision: Apostomatia: [42]; Apostomatida: [43]; *Trichodina*: [44]; *Epistylis* and *Opercularia*: [45]; *Spirochona*: [46]; *Buetschlia* and *Charonina*: [31, 47–51]. Life cycles, encystment/excystment process: [52–54]. Pathogenicity, damages, infestation degree, virulence: [55–59]. Molecular and phylogeny: [30, 60–68]. Ecological aspects: [69, 70]. Immunity: [71, 72]. Stomatogenesis: [73]. Ultrastructure: [74].

Symbiotic systems between ciliates/animals are present in a broad spectrum of kingdom Animalia, and some examples are the following (animal group alphabetically arranged, different taxonomic levels): acari: [75]; amphipods: [76]; antilope: [77]; anuran: [78]; Asian elephant: [79]; baboon: [80]; bryozoans: [81]; buffaloes: [82]; capybara: [83–85]; cattle: [86]; chimpanzees: [87]; cirripedians: [88]; crustaceans: [89]; ctenophores: [90]; cuttlefish: [91]; dromedary camels: [92]; elephants: [93]; fishes: [94, 95]; frogs: [96]; great apes: [97]; horses: [98, 99]; humans: [100, 101]; polyps of hydras: [102]; insects: [103]; isopods: [104, 105]; kinorhynchs: [106]; llamas: [107]; maccacus: [108]; mammals: [109]; mollusks: [71, 76]; nematodes: [29, 110]; nemerteans: [13]; oligochaetes: [111, 112]; ostracods: [113]; polychaetes: [114, 115]; rhinoceroses: [116]; sea urchins: [117]; thoroughbreds: [118]; turbellarians: [119]; wood-feeding roaches: [120].

Some examples of ciliate taxa that include symbiotic species are the following: **Heterotrichea:** Folliculinids attach to the integument of various invertebrates as bivalve shells, crustaceans exoskeleton, polychaete tubes, hydroid perisarcs, bryozoan tests, with a widespread occurrence [121], and may cause the skeletal eroding band or brown band diseases of scleractinian corals [2]; their life cycle includes a

migratory swimming stage. **Spirotrichea:** Hypotrichs are known mainly as free-living organisms, but some species such as *Euplotes balteatus* have been recorded in some sea urchins' intestinal tract [122]. Some species of stichotrichids as *Plagiotoma lumbrici* are endosymbionts of oligochaetes [123].

**Armophorea:** Class Armophorea includes clevellandellids as Nyctotheridae, with obligate endosymbionts usually as commensals of invertebrates and vertebrates; life cycles include a phase of the cyst [2].

**Litostomatea:** Trichostomes are symbionts of vertebrates as ruminants and foregut fermenters [2], including the human pathogen, *Balantidium coli*, species that have a life cycle including two phases: trophozoites and cysts [25]. This species

#### *Ciliates as Symbionts DOI: http://dx.doi.org/10.5772/intechopen.99341*

has been considered to be included in a new genus, *Neobalantidium coli* [124]. The genus *Balantidium* has a more significant number of species that have been reported as endocommensals in the digestive tracts of a widely diverse range of metazoan, as mollusks, arthropods, fishes, reptiles, birds, and mammals [124]. In the rumen ecosystem, ciliates can account for up to 50% of the total microbial nitrogen, reaching densities of 105 to 106 cells/ml rumen fluid, being *Charonina ventriculi* one of the smallest rumen ciliates [125].

Ophryoscolecidae and Cycloposthiidae include species as endosymbionts of ruminants and equids, respectively [126]. Entodiniomorphid ciliates of the genus *Triplumaria* are found in the intestine of elephants and rhinoceroses [60]. Entodiniomorphida do not form cysts, and in non-ruminant mammals, the infections of hosts occur by coprophagy [47].

**Phyllopharyngea:** Chonotrichs live on marine and freshwater hosts and divide by forming external or internal buds [127], with a dimorphism where the adults live attached to several appendages of crustaceans, and the larva is free and swims to reach a new host [128].

Suctorians, as a rule, reproduce by different modes of budding, produce one to several larvae, with a short swimming existence, and then lose their cilia and metamorphose into adults or trophonts [127]. The non-ciliated mature stages of suctorians are usually sessile, attached to the substrate by a non-contractile stalk, and reproduce by ciliary larvae called swarmers or migrators [129].

**Oligohymenophorea:** Yi et al. [130] documented that the life cycle of *Ichthyophthirius multifiliis*, a parasite of fish, consists of three key developmental stages: the infective theront, the parasitic trophont, and the reproductive tomont.

*Mesanophrys pugettensis*, is a scuticociliate thata was observed with a diphasic life history, the larger phase or trophont, and the smaller phase resembling tomites [34], is a facultative parasite of the Dungeness crab. *Conchophthirus* species are generally considered an endocommensal inhabiting the mantle cavity of freshwater clams or mussels [30].

Thigmotrichids from several families were analyzed by Raabe [131–134], where species of Hemispeiridae are symbionts of the mantle cavity and nephridia of molluscan, those of Ancistrocomidae, Sphenopryidae and Thigmophryidae are ectosymbionts of mantle cavity and gills of molluscan, and Hysterocinetidae species were categorized as endoparasites of the gut of prosobranch mollusks; life cycles include tomites.

The apostomes is a small group of oligohymenophorean ciliates, with four major life histories: 1-exuviotrophic, that remain encysted on the exoskeleton of a crustacean host, and excyst to feed on exuvial fluid, reproducing during the host ecdysis, 2-sanguicolous, penetrate the cuticle of the host, feed on the cells and fluid of the hemocoel and reproduces, 3-chromidinid, found in the renal organs and opalinopsids found in the liver and intestines of cephalopods ingesting fluids and cells, 4-histotrophs, such as *Vampyrophrya* [135]. Apostome ciliates have life cycles typically involving crustaceans, with a non feeding microstome tomite and a macrostomous trophont [127]. Species of apostome of genus *Collinia* are endoparasites able to reproduce rapidly within the host that invariably kill the euphausiid within 40 hours of infection; *Gymnodinioides* genus includes exuviotrophic species that feed on the fluid within the exuviae of crustacean hosts and Landers *et al*., [136] documented for *Gymnodinioides pacifica* the presence of trophonts, phoronts, tomonts and tomites. For *Synophrya* the phoront, hypertrophont, hypertomont, and hypertomites were observed [137].

Pilisuctorian ciliates spend most of their lives perched on cuticular setae of crustaceans, and complete their life cycle on a single host, having the stages tomite, tomont and trophont [138].

In peritrichs, a significant character is the scopula which is the region that originates the stalk to attach the organism to the substrate and modifies to a highly complicated adhesive apparatus in mobiline [127]; two phases are known, the trophont and the dispersive telotroch.

Species of sessile peritrichs genera such *Ambiphrya*, *Epistylis*, *Heteropolaria*, *Rhabdostyla*, and *Zoothamnium* are epibionts of zooplanktonic invertebrates, larval stages of aquatic insects, aquatic mollusks, crustaceans, fish, amphibians, and reptiles as the main groups of organisms [139]. Members of genus *Epistylis* have been reported as epibionts in several metazoans, but also as an important fish ectoparasite being considered an emerging pathogen [140]. Genus *Lagenophrys* comprises only symbiotic species of freshwater and marine crustaceans [89]. Trichodinids are the most devastating ectoparasites of cultured fish, causing severe damage [141], and for genus *Trichodina* about 300 species have been described, mostly from freshwater environments [142]. Also, there are reports of trichodinids from the gills of limpets [143] and have been documented as symbionts of a broad spectrum of aquatic and terrestrial invertebrates and vertebrates hosts [65]. *Trichodinella epizootica* is one of the most widely distributed freshwater trichodinids in Europe and Asia, but has also been reported from Africa, the Pacific region and North America [55]. *Urceolaria* includes species ectosymbionts of freshwater turbellarians, marine polychaetes, and mollusks; *Leiotrocha* species are ectocommensals and endocommensals of marine molluscans, and species of *Polycycla* are endocommensals of Holothuroidea [144].
