Abstract
The study of ciliate diversity in tropical environments remains scarce. In Neotropical forests, bromeliads are a common component of the vascular flora; bromeliads with tank morphology intercept rain water and detritus, resulting in the formation of a phytotelm, where heterotrophic protist communities like ciliates can establish. However, it is not known if ciliates inhabit tank-less bromeliads. For this reason, the goal of the present study was to investigate if ciliates can establish between the leaf axils of five terrestrial and epiphytic tank-less bromeliad species in a dry tropical forest in west Mexico. We collected samples of rain water and detritus from the leaf axils during the humid season of years 2015 and 2016. For ciliate taxonomical identification, we used optical microscopy, in vivo observation, and silver impregnation techniques. To summarize information about geographical distribution of ciliates identified at species level in the Neotropics, we provided their records from previous works, at country level with locality and georeferenciation. We recorded 27 taxa of ciliates, where the class Oligohymenophorea contained the largest richness of taxa. Drepanomonas revoluta, Leptopharynx bromeliophilus, and Tetrahymena sp. were recorded from all the species of bromeliads. Bromelia karatas was the species that hosted the largest number of ciliate taxa (22). Our results indicated that Glaucomides bromelicola, Gonostomum bromelicola, Leptopharynx bromelicola and L. bromeliophilus, species which are considered endemic to tank bromeliads, can also inhabit tank-less bromeliads. We provided previous records of 19 ciliate species from eleven countries within the Neotropical region, and Bromeliothrix metopoides was the species most frequently recorded in Neotropical countries (9). Therefore, tank-less bromeliads can constitute a temporal habitat for ciliates, and function as cysts reservoirs in environments with a pronounced seasonality like dry tropical forests.
References
Aladro-Lubel, M.A., Martínez-Murillo, M.E. & Mayén-Estrada, R. (1990) Manual de ciliados psamófilos marinos y salobres de México. Instituto de Biología, Universidad Nacional Autónoma de México, México, 172 pp.
Aladro-Lubel, M.A., Mayén-Estrada, R. & Reyes-Santos, M. (2006) Listados Faunísticos de México XI. Registro Actualizado de Ciliados. Agosto, 2004. Instituto de Biología, Universidad Nacional Autónoma de México, 97 pp.
Arévalo-Trear, R.E. (1967) Sistemática y morfología de algunas especies de protozoarios edafícolas aislados de un tipo de suelo de andosol, del estado de Morelos, México. Undergraduated thesis, Universidad Nacional Autónoma de México, 41 pp.
Benzing, D.H. (2000) Bromeliaceae: profile of an adaptive radiation. Cambridge University Press, New York, 655 pp.
https://doi.org/10.1017/CBO9780511565175
Berger, H. (1999) Monograph of the Oxytrichidae (Ciliophora, Hypotrichia). Monographiae Biologicae 78, Dordrecht, Netherlands, 1079 pp.
Bourland, W. (2017) How far do ciliate flagships sail? A proposed Gondawanaland endemic species at anchor in Idaho soils. Protist, 168 (3), 352–361.
https://doi.org/10.1016/j.protis.2017.04.002
Bovee, E. (1957) Protozoa of Amazonian and Andean waters of Colombia, South America. Journal of Protozoology, 4, 63–66.
https://doi.org/10.1111/j.1550-7408.1957.tb02487.x
Buosi, P.R.B., Utz, L.R.P., de Meira, B.R., Segóvia da Silva, B.T., Lansac-Tôha, F.M., Lansac-Tôha, F.A.L. & Velho, L.F.M. (2014) Rainfall influence on species composition of the ciliate community inhabiting bromeliad phytotelmata. Zoological Studies, 53, 1–12.
https://doi.org/10.1186/s40555-014-0032-4
Bütschli, O. (1887-1889) Protozoa. Abt. III. Infusoria und System der Radiolaria. In: Bronn, H.G. (Ed.), Klassen und Ordnung des Thiers Reichs Vol. 1, C.F. Winter, Leipzig, pp. 1089–2035.
Ceballos, G. & García, A. (1995) Conserving neotropical biodiversity: the role of dry forests in western Mexico. Conservation Biology, 9, 1349-–1356.
Certes, A. (1891) Note sur deux infusoires nouveaux des environs de Paris. Mémoires de la Société Zoologique de France, 4, 536–541.
Cruz-Jiménez, G. (2017) Riqueza de ciliados (Protozoa: Ciliophora) que habitan en Campylopus pilifer Brid. (Bryophyta) en un gradiente altitudinal en el estado de Oaxaca. Undergraduated thesis, Universidad de la Sierra Juárez, Mexico, 69 pp.
Dragesco, J. & Dragesco-Kernéis, A. (1979) Ciliès muscicoles nouveaux ou peu connus. Acta Protozoologica, 18, 401–416.
Dragesco, J. & Dragesco-Kernéis, A. (1986) Ciliés libres de l'Afrique intertropicale: introduction à la connaissance et à l'étude des Ciliés. Editions de l’Orstom, Paris, 559 pp.
Dunthorn, M., Stoeck, T., Wolf, K., Breiner, H.W. & Foissner, W. (2012) Diversity and endemism of ciliates inhabiting Neotropical phytotelmata. Systematics and Biodiversity, 10 (2), 195–205.
https://doi.org/10.1080/14772000.2012.685195
Durán-Ramírez, C.A., García-Franco, J.G., Foissner, W. & Mayén-Estrada, R. (2015) Free living ciliates from epiphytic tank bromeliads in Mexico. European Journal of Prostistology, 51, 15–33.
https://doi.org/10.1016/j.ejop.2014.09.002
Enriques, P. (1908) Sulla morfologia e sistematica del genere Colpoda. Archives de Zoologie Expérimentale et Générale, 8, 1–15.
Espejo Serna, A. & López-Ferrari, A.R. (2005) Una nueva especie de Tillandsia (Bromeliaceae) del Occidente de México. Acta Botánica Mexicana, 72, 53–64.
https://doi.org/10.21829/abm72.2005.1001
Espejo-Serna, A., López-Ferrari, A.R., Ramírez-Morillo, I., Holst, B.K., Luther, H. & Hill, W. (2004) Checklist of Mexican Bromeliaceae with notes on species distribution and levels of endemism. Selbyana, 25, 33–86.
Fernández-Galiano, D. & Calvo, P. (1992) Redescription of Phacodinium metchnikoffi (Ciliophora, Hypotrichida): general morphology and taxonomic position. Journal of Protozoology, 39 (4), 443–448.
https://doi.org/10.1111/j.1550-7408.1992.tb04829.x
Foissner, W. (1987a) Soil protozoa: fundamental problems, ecological significance, adaptations in ciliates and testaceans, bioindicators, and guide to the literature. Progress in Protistology, 2, 69–212.
Foissner, W. (1987b) Neue und wenig bekannte hypotriche und colpodide Ciliaten (Protozoa: Ciliophora) aus Böden und Moosen. Zoologische Beiträgen N. F., 31 (2), 187–282.
Foissner, W. (1993) Colpodea (Ciliophora). Gustav Fischer Verlag. New York, 789 pp.
Foissner, W. (1995) Tropical protozoan diversity: 80 ciliate species (Protozoa, Ciliophora) in a soil sample from a tropical dry forest of Costa Rica, with descriptions of four new genera and seven new species. Archiv für Protistenkunde, 145, 37–79.
https://doi.org/10.1016/S0003-9365(11)80300-3
Foissner, W. (1997) Soil ciliates (Protozoa: Ciliophora) from evergreen rain forests of Australia, South America and Costa Rica: diversity and description of new species. Biology and Fertility of Soils, 25, 317–339.
https://doi.org/10.1007/s003740050322
Foissner, W. (1998) An updated compilation of world soil ciliates (Protozoa, Ciliophora), with ecological notes, new records, and descriptions of new species. European Journal of Protistology, 34, 195–235.
https://doi.org/10.1016/S0932-4739(98)80028-X
Foissner, W. (2000) Notes on ciliates (Protozoa, Ciliophora) from Espeletia trees and Espeletia soils of the Andean Páramo, with descriptions of Sikorops espeletiae nov. spec. and Fragmocirrus espeletiae nov. gen., nov. spec. Studies on Neotropical Fauna and Environment, 35, 52–79.
https://doi.org/10.1076/0165-0521(200004)35:1;1-M;FT052
Foissner, W. (2008) Protist diversity and distribution: some basic considerations. Biodiversity and Conservation, 17, 235–242.
https://doi.org/10.1007/s10531-007-9248-5
Foissner, W. (2010) Life cycle, morphology, ontogenesis, and phylogeny of Bromeliothrix metopoides nov. gen., nov. spec., a peculiar ciliate (Protista, Colpodea) from tank bromeliads (Bromeliaceae). Acta Protozoologica, 49 (3), 159–193.
Foissner, W. (2013) Description of Glaucomides bromelicola n. gen., n. sp. (Ciliophora, Tetrahymenida), a macrostome-forming inhabitant of bromeliads (Bromeliaceae), including redescriptions of Glaucoma scintillans and G. reniformis. Journal of Eukaryotic Microbiology 60, 137–157.
https://doi.org/10.1111/jeu.12016
Foissner, W. (2014) An update of basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa. International Journal of Systematic and Evolutionary Microbiology, 64, 271–292.
https://doi.org/10.1099/ijs.0.057893-0
Foissner, W. (2016) Terrestrial and semiterrestrial ciliates (Protozoa, Ciliophora) from Venezuela and Galápagos. Denisia, 35, 1–912.
Foissner, W., Strüder-Kypke, M., van der Staay, G., Moon-van der Staay, S. & Hackstein, J. (2003) Endemic ciliates (Protozoa, Ciliophora) from tank bromeliads (Bromeliaceae): a combined morphological, molecular, and ecological study. European Journal of Protistology, 39, 365–372.
https://doi.org/10.1078/0932-4739-00005
Foissner, W., Wolf, K.W., Yashchenko, V. & Stoeck, T. (2011) Description of Leptopharynx bromelicola n. sp. and characterization ofthe genus Leptopharynx Mermod, 1914 (Protista, Ciliophora). Journal of Eukaryotic Microbiology, 58, 134–151.
https://doi.org/10.1111/j.1550-7408.2011.00532.x
García-Oliva, F., Maass, J. M. & Galicia, L. (1995) Rainstorm analysis and rainfall erosivity of a seasonal tropical region with a strong cyclonic influence in the Pacific Coast of Mexico. Journal of Applied Meteorology, 34, 2491–2498.
https://doi.org/10.1175/1520-0450(1995)034<2491:RAAREO>2.0.CO;2
Givnish, T.J., Barfuss, M.H., Van Ee, B., Riina, R., Schulte, K., Horres, R., Gonsiska, P.A., Jabaily, R.S., Cray, D.M., Smith, J.A.C., Winter, K., Brown, G.K., Evans, T.M., Holst, B.K., Luther, H., Till, W., Zizka, G., Berry, P.E. & Sytsma, K.J. (2014) Adaptive radiation, correlated and contingent evolution, and net species diversification in Bromeliaceae. Molecular Phylogenetics and Evolution 71, 55–78.
https://doi.org/10.1016/j.ympev.2013.10.010
Givnish, T.J., Millam, K. C., Berry, P.E. & Sytsma, K.J. (2007) Phylogeny, adaptive radiation, and historical biogeography of Bromeliaceae inferred from ndhF sequence data. Journal of Systematic and Evolutionary Botany, 23 (1), 3–26.
Gouda, E.J., Butcher, D. & Gouda, C.S. (2015) Encyclopaedia of Bromeliads, Version 3. University Botanic Gardens, Utrecht. Available from: http://encyclopedia.florapix.nl/ (accessed 27 November 2017)
Gmelin, J.F. (Ed.) (1790) Caroli Lineé Systema Naturae per regna tria naturae, secundum classes, ordines, genere, species, cum characteribus differentiis, synonymis, locis. Ed. 13, Leipzig, 500 pp.
Guggiari, M. & Peck, R. (2008) The bacterivorous ciliate Cyclidium glaucoma isolated from a sewage treatment plant: molecular and cytological descriptions for barcoding. European Journal of Protistology, 44 (3), 168–180.
https://doi.org/10.1016/j.ejop.2007.11.004
Hardoim, E.L. & Heckman, C.W. (1996) The seasonal succession of biotic communities in wetlands of the tropical wet and dry climatic zone: IV. The free living sarcodines and ciliates of the Pantanal of Mato Grosso, Brazil. International Review of Hydrobiology, 81 (3), 367–384.
https://doi.org/10.1002/iroh.19960810307
Hernández-Anaya, M. (1981) Ciliados de una laguneta de los médanos cercanos al puerto de Veracruz. Undergraduated thesis, Universidad Nacional Autónoma de México, México, 81 pp.
Kahl, A. (1926) Neue und wenig bekannte Formen der holotrichen und heterotrichen Ciliaten. Archive für Protistenkunde, 55, 197–438.
Küppers, G.C. & Claps, M.C. (2012a) Freshwater ciliates (Protozoa, Ciliophora) from Argentina: an annotated and updated compilation. In: Thangadurai, D., Busso, C.A., Abarca-Arenas, L.G. & Jayabalan, S. (Eds.), Frontiers in Biodiversity Studies. I.K. International Publishing House, New Delhi and Bangalore, India, pp. 61–100.
Küppers, G.C. & Claps, M.C. (2012b) Spatiotemporal variations in abundance and biomass of planktonic ciliates related to environmental variables in a temporal pond, Argentina. Zoological Studies, 51 (3), 298–313.
Küppers, G.C. & Claps, M.C. (2016) Diversity of freshwater ciliates (Protista) from Argentina. Revista Brasileira de Zoociências, 17 (1), 63–76.
Lee, J.J., Leedale, G.F. & Bradbury, P. (2000) An illustrated guide to the Protozoa. Vol. I. Society of Protozoologists, Kansas, 689 pp.
Lynn, D.H. (2008) The ciliated protozoa: characterization, classification, and guide to the literature. Springer, Dordrecht. Netherlands, 605 pp.
Madrazo-Garibay, M. & López-Ochoterena, E. (1982) Segunda lista taxonómica comentada de protozoarios de vida libre de México. Revista Latinoamericana de Microbiología, 24, 281–295.
Madrazo-Garibay, M. & López-Ochoterena, E. (1985) Protozoarios ciliados de México XXVI. Análisis morfológico y taxonómico de treinta y cinco especies de la laguna de Términos, Campeche. Anales del Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México 12, 199–212.
Maguire, Jr. B. (1971) Phytotelmata: biota and community structure determination in plant-held waters. Annual Reviews in Ecology and Systematics, 2, 439–464.
https://doi.org/10.1146/annurev.es.02.110171.002255
Maupas, E. (1883) Contribution à l'etude morphologique et anatomique des infusoires ciliés. Archives de Zoologie Expérimentale et Générale (Ser. 2), 11, 427–664.
Méndez-Sánchez, D. (2017) Estudio taxonómico de ciliados de vida libre (Alveolata: Ciliophora) en cuerpos de agua dulce de dos regiones biogeográficas de México. Master’s thesis, Universidad Nacional Autónoma de México, México, 149 pp.
Mermod, G. (1914) Recherches sur la faune infusorienne des tourbieres et des eaux voisines de Sainte-Croix (Jura vaudois). Revue Suisse de Zoologie, 22, 31–114.
https://doi.org/10.5962/bhl.part.36669
Mondragón-Camarillo, L. (2011) Estructura trófica de la comunidad de ciliados y flagelados en un suelo de cultivo contaminado con combustóleo de Jalacingo, Veracruz. Master’s thesis, Universidad Nacional Autónoma de México, México, 56 pp.
Morrone, J.J. (2017). Neotropical biogeography: Regionalization and evolution. CRC Press. Florida, 282 pp.
Müller, O.F. (1773) Vermium terrestrium et fluviatilium, seu animalium infusorium, helminthicorum et testaceorum, non marinorum, succincta historia. Heineck & Faber, Hafniae & Lipsiae, pp. l–30, 1–135.
Omar, A. & Foissner, W. (2011) Description of Leptopharynx bromeliophilus nov. spec. and Leptopharynx australiensis nov. spec. (Ciliophora, Nassulida). Acta Protozoologica, 50 (2), 89–103.
Omar, A. & Foissner, W. (2012a) Neotypification and ontogenesis of Leptopharynx costatus costatus Mermod, 1914. Journal of Eukaryotic Microbiology, 59 (3), 268–286.
https://doi.org/10.1111/j.1550-7408.2012.00620.x
Omar, A. & Foissner, W. (2012b) Description of Leptopharynx brasiliensis nov. spec. and Leptopharynx costatus gonohymen nov. subspec. (Ciliophora, Microthoracida). European Journal of Protistology, 48 (1), 30–47.
https://doi.org/10.1016/j.ejop.2011.07.002
Omar, A. & Foissner, W. (2014) Three new microthoracids (Ciliophora, Nassophorea) from Austria and Venezuela. Acta Protozoologica, 53, 295–311.
Pauleto, G.M., Velho, L.F.M., Buosi, P.R.B., Brão, A.F.S., Lansac-Tôha, F.A. & Bonecker, C.C. (2009) Spatial and temporal patterns of ciliate species composition (Protozoa: Ciliophora) in the plankton of the Upper Paraná River floodplain. Brazilian Journal of Biology, 69 (2), 517–527.
https://doi.org/10.1590/S1519-69842009000300007
Penard, E. (1922) Études sur les infusoires d'eau douce. Georg & Cie Ed., Genève, 331 pp.
Prowazek, S. von (1900) Protozoenstudien II. Arbeiten aus dem Zoologischen Instituten der Universität Wien, 12, 243–300.
Reyes‐García, C., Mejia‐Chang, M. & Griffiths, H. (2012) High but not dry: diverse epiphytic bromeliad adaptations to exposure within a seasonally dry tropical forest community. New Phytologist, 193 (3), 745–754.
https://doi.org/10.1111/j.1469-8137.2011.03946.x
Rico-Ferrat, G. (1990) Identificación de los protozoarios que habitan en la hojarasca de un bosque mesófilo en Gómez Farías, Tamaulipas, México. Revista de la Sociedad Mexicana de Historia Natural, 41, 33–36.
Rondello-Bonatti, T., Siqueria-Castro, I.C.V. & Bueno-Franco, R.M. (2016) Checklist of ciliated protozoa from surface water and sediment samples of Atibaia River, Campinas, São Paulo (Southeast Brazil). Revista Brasileira de Zoociências, 17 (1), 63–76.
Sigala-Regalado, I. (2011) Diversidad de protozoos ciliados en cinco biotopos de cuevas en México. Master’s thesis, Universidad Nacional Autónoma de México, México, 130 pp.
Small, E.B. (1967) The Scuticociliatida, a new order of the class Ciliatea (phylum Protozoa, subphylum Ciliophora). Transactions of the American Microscopical Society, 86 (4), 345–370.
https://doi.org/10.2307/3224258
Steffens, S. & Wilbert, N. (2002) Ciliates (Protozoa: Ciliophora) of selected ephemeral flushs on tropical inselbergs. International Review of Hydrobiology, 87 (4), 401–410.
https://doi.org/10.1002/1522-2632(200207)87:4<401::AID-IROH401>3.0.CO;2-A
Trejo, I. (2010). Las selvas secas del Pacífico mexicano In: Ceballos, G., Martínez, L., García, A., Espinoza, E., Creel, J.B. & Dirzo, R. (Eds.), Diversidad, amenazas y áreas prioritarias para la conservación de las selvas secas del Pacífico de México. EcoCiencia, S. C., CONANP, FCE, CONABIO, TELMEX, Telcel, WWF, México, pp. 42–51.