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Corresponding author: Mireya Ramírez-Ballesteros ( mballesteros@ciencias.unam.mx ) Academic editor: Ingo S. Wehrtmann
© 2018 Mireya Ramírez-Ballesteros, Gregorio Fernandez-Leborans, Rosaura Mayén-Estrada.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Ramírez-Ballesteros M, Fernandez-Leborans G, Mayén-Estrada R (2018) New record of Epistylis hentscheli (Ciliophora, Peritrichia) as an epibiont of Procambarus (Austrocambarus) sp. (Crustacea, Decapoda) in Chiapas, Mexico. ZooKeys 782: 1-9. https://doi.org/10.3897/zookeys.782.26417
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Epibiosis is very common between crustaceans and ciliates where the calcified surface of the crustacean body provides a suitable substrate for ciliate colonization. The aim of this contribution is to provide data about a new record between the epistylid ciliate Epistylis hentscheli Kahl, 1935, and the crayfish Procambarus (Austrocambarus) sp. The distribution of the epistylid on the basibiont body and its cellular/colonial characteristics were analyzed. Procambarus (Austrocambarus) sp. harbored colonies of E. hentscheli only on the pereiopods. This is the first record of this peritrich ciliate as an epibiont on Crustacea, having been previously found on algae and fish.
ciliate, colonies, epibiosis, epistylid, Montebello
Epibiosis is a facultative and interspecific association between two organisms, the epibiont and the basibiont, the latter providing a substrate for the attachment of the former (
Epibiotic associations between crustaceans and ciliates are very common, since the calcified surface of the crustacean functions as a semi-permanent substrate, providing an optimal habitat for epibionts ciliates, especially in those areas where other substrates are not suitable for long-term colonization (
Ciliates of the genus Epistylis include colonial organisms with a non-contractile and branched stalk; each zooid has a well-defined peristomial lip and epistomial disc in the oral region, being the zooids elongated and generally in the shape of a vase (
The goal of this contribution is to provide data of E. hentscheli and its distribution on the body of the crayfish Procambarus (Austrocambarus) sp., including some cellular/colonial characteristics of the epistylid.
Species of the genus Epistylis reported previously as epibionts of freshwater decapods.
Decapod host | Ciliate species | Infected body regions | Sources |
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Pontastacus leptodactylus Eschscholtz, 1823 | Epistylis sp. | Antennae Carapace Pleopods Telson Uropods Gills |
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E. niagarae Kellicott, 1883 | |||
E. chrysemidis Bishop & Jahn, 1941 | |||
E. astaci Nenninger, 1948 | |||
E. cambari Kellicott, 1885 | |||
E. crassicollis Stein, 1867 | |||
Astacus astacus Linnaeus, 1758 | E. astaci | Rostrum Antennules Antennae |
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E. bimarginata Nenninger, 1948 | |||
E. crassicollis | |||
Cherax tenuimanus Smith, 1912 | Epistylis sp. | Pereiopods |
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Cambarellus patzcuarensis Villalobos, 1943 | E. bimarginata | Uropod Antennules Rostrum Gill Pereiopods Pereiopod Uropod Telson |
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E. branchiophila Perty-Stein, 1859 | |||
E. carinogammari Stiller, 1949 | |||
E. gammari Precht,1935 | |||
E. lacustris Imhoff, 1884 | |||
E. niagarae | |||
E. stammeri Nenninger, 1948 | |||
E. variabilis Stiller, 1953 |
Sampling. Specimen of Procambarus (Austrocambarus) sp. were collected in an artificial pond of Montebello Chiapas, Mexico [16°04.40N, 91°37.40W (DDM)], 1,507 m above sea level, during the rainy and dry seasons in years 2014–2015, being the mud and clay the principal substrate. Collections during the rainy season and the dry season were performed every three months, and in each sampling the following physical and chemical parameters were measured: water temperature, conductivity, and pH by a YSI model 85 multiparameter sonde and dissolved oxygen concentration was measured with an oximeter YSI model 55/12.
Technique procedures. Crustaceans were transported alive to the Protozoology laboratory (Faculty of Sciences, Universidad Nacional Autónoma de México, Mexico City), and maintained alive in aquaria. Specimens were later dissected to separate the telson, pleopods, pereiopods, carapace, chelipeds, antennae, eyes, gills, and mouthparts. Peritrichs were observed with a Nikon stereoscopic microscope (SMZ 800). Photomicrographs and morphometric records were obtained using a Nikon digital camera (Digital Sight DS2Mv) adapted to a Nikon microscope (Labophot2/AX70).
Ciliates were fixed in 70% alcohol, to reveal their cellular structure with the pyridine silver carbonate technique (
The physical and chemical parameters data recorded during the dry (DS) and rainy season (RS) of the pond, which were measured each three months were: temperature (DS: 18.7 °C ± 2.1, RS: 21.2 °C ± 1.8), pH (DS: 7 ± 0.5, RS 6 ± 0.4) conductivity (DS: 321 µS ± 56, RS: 243 µS ± 64), and dissolved oxygen (DS: 7.46 mg/L ± 0.9, RS:8.85 mg/L ± 0.87).
Ninety-six crayfish specimens were collected, 46 in the dry season and 50 in the rainy season. Epistylis hentscheli was recorded only during the dry season of year 2015 on 36 individuals of the crayfish (prevalence of 78%), and only on pereiopods, between the merus and the carpus (Figure
Forty colonies of E. hentscheli with 20–30 zooids were observed with a dichotomously branched pattern, with a long and rigid main stalk that contained peripheral fibers arranged longitudinally (Figure
From stained zooids we observed one spherical micronucleus located close to the central macronucleus (Figure
A–B Epistylis hentscheli in vivo, A colony B detail of zooid C–F zooid after silver carbonate staining C details of myonemes and macronucleus D details of stalk E detailed longitudinal fibers in the stalk F colony showing contracted zooids G–I protargol-stained zooids. Abbreviations: Cv. contractile vacuole; H. haplokinety; M. myonemes; Mac. macronucleus; Mi. micronucleus; Po. polykinety; Sc. scopula; Sm. stretch marks. Scale bars: 100 µm (A), 25 µm (B–D, F–H), and 10 µm (E, I).
Biometric features of Epistylis hentscheli in vivo and after protargol staining, colonizing Procambarus (Austrocambarus) sp. (measurements in µm, n=38; Min. minimum; Max. maximum; S.D. standard deviation; C.V. coefficient of variation).
Attribute | Measurements in vivo | Measurements after protargol staining | ||||||||
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Min. | Max. | Mean | S.D. | C.V | Min. | Max. | Mean | S.D. | C.V | |
Zooid length | 111 | 140 | 120 | 21.4 | 0.17 | 32 | 76 | 54 | 14.6 | 0.27 |
Zooid width | 58 | 87 | 73 | 9.85 | 0.13 | 65 | 91 | 78 | 7.43 | 0.09 |
Width of peristomial collar | 62 | 90 | 76 | 9.71 | 0.12 | 20 | 34 | 28 | 4.06 | 0.14 |
Macronucleus width | 4 | 6 | 5 | 0.88 | 0.17 | 3 | 5 | 4 | 0.81 | 0.20 |
Macronucleus length | 37 | 44 | 40 | 2.46 | 0.06 | 25 | 34 | 30 | 3.05 | 0.10 |
Primary stalk length of colony | 511 | 700 | 606 | 62.7 | 0.10 | 511 | 700 | 606 | 62.7 | 0.10 |
Primary stalk width of colony | 7.3 | 7.5 | 7.4 | 0.08 | 0.01 | 7.3 | 7.5 | 7.4 | 0.08 | 0.01 |
The current study represents the first ever record of Epistylis hentscheli as an epibiont of Crustacea. Some ciliate species have been recorded on decapods in Mexico (López-Ochoterena and Ochoa-Gasca 1971;
Epistylis hentscheli colonies were formed by 20–30 zooids each and were attached to the pereiopods of Procambarus (Austrocambarus) sp. It is likely that the constant movement of these pereiopods provide a constant water flow carrying suspended food particles and oxygen to the ciliates. In contrast, the dorsal surface of the basibiont is subject to comparatively little water flow and also is exposed to more abrasion forces, possibly preventing the ciliate attachment. The ciliate colonies of E. hentscheli on the pereiopods were very long, with a stalk of 600 μm. This result agrees with that of
Epibiosis is a facultative association, in which both participants gain advantages but also have disadvantages from this interaction (
We are grateful to the Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, and CONACyT for a grant to MRB for master’s degree. We are indebted to Dr. Villalobos-Hiriart (Instituto de Biología, UNAM) for the crustacean identification, and to M. en A. Aldi de Oyarzabal-Salcedo (Facultad de Ciencias, UNAM) for the scientific illustration. We also appreciate the technical support of Margarita Reyes-Santos (Facultad de Ciencias, UNAM), María Valladolid and Manuela Gallardo (Museo de Ciencias Naturales, CSIC). Special thanks to Dr. Alan Warren (Natural History Museum, Department of Life Sciences, UK) for his comments and assistance with the English. Finally, our sincere thanks to the people of Tziscao village for allowing us to work in their community.