New record of Epistylis hentscheli (Ciliophora, Peritrichia) as an epibiont of Procambarus (Austrocambarus) sp. (Crustacea, Decapoda) in Chiapas, Mexico
New record of Epistylis hentscheli (Ciliophora, Peritrichia) as an epibiont of Procambarus (Austrocambarus) sp. (Crustacea, Decapoda) in Chiapas, Mexico
Mireya Ramírez-Ballesteros 0
Rosaura Mayén-Estrada 0
0 Laboratorio de Protozoología, Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México , Av. Universidad 3000, Circuito Exterior S/N. Coyoacán , 04510. Ciudad de México, México 2 Posgrado en Ciencias Biológicas, Facultad de Ciencias, Universidad Nacional Autónoma de México 3 Departamento de Zoología, Facultad de Biología, Universidad Complutense , Calle José Antonio Novais 12, 28040. Madrid , España
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.
eol>ciliate; colonies; epibiosis; epistylid; Montebello
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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
. The basibionts are usually significantly larger than epibionts, have
body surfaces that are physiologically inactive, and are sessile or slow-moving
(Threlkeld et al. 1993; Wahl and Mark 1999)
. Epibiosis is a continuous and dynamic process
in which the benefits and costs for basibionts and epibionts can change depending on
environmental conditions (Fernandez-Leborans 2010).
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
. Among the
ciliate epibionts of crustaceans, the Peritrichia
(Fernandez-Leborans and Tato-Porto
(Batisse 1994; Fernandez-Leborans and Tato-Porto 2000b)
are the most commonly reported. Regarding
the 13 species of the sessilid peritrich genus Epistylis (Table 1), so far there have been
no reports of E. hentscheli as epibiont of crustaceans.
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
. Procambarus (Austrocambarus) sp., a member of the family Cambaridae, is a
freshwater decapod inhabiting dams, streams, and rivers. Species of this genus are
considered important macro- invertebrates in temperate and tropical areas, participating in
maintaining the balance in the food chain through the processes of degradation of the
organic matter of the systems
(Álvarez et al. 2012; Yazicioglu et al. 2016)
. The crayfish
can represent up to 85% of the zoobenthic biomass, are considered strong engineers of
the ecosystems, and can be considered as ecological regulators (
Veselý et al. 2015
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.
Materials and methods
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
(Fernandez-Leborans and Castro 1986)
, and the
protargol impregnation technique
. Peritrichs measurements were
obtained from live and stained individuals and included: length and width of the zooid,
macronucleus, stalk and also width of the peristomial collar. Epistylis hentscheli was
identified based on morphological characteristics described by
Foissner et al. (1992)
including the measurements of length and width of the zooids, and the width of the
peristomial collar. Main morphological features of this species include the shape of the
zooids and tall of the entire colony.
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 1); the number of colonies on individual
crayfish varied between one and three.
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 2E). The observation of 38 zooids in vivo
showed uncontracted and trumpet-shaped zooids (Figure 2A, B), with a peristomial
disc slightly raised above the peristome; and with the infundibulum reached more than
half the length of the zooid (Figure 2B). The single contractile vacuole was located
above the C-shaped macronucleus (Figure 2B, D).
From stained zooids we observed one spherical micronucleus located close to the
central macronucleus (Figure 2G). The oral infraciliature comprised the haplokinety
and polykineties running parallely, which made approximately one and a quarter turns
around the peristomial disc. At the opening of the infundibulum the haplokinety
separated from the polykinety (Figure 2H–I). Biometric data of E. hentscheli are shown in
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
(LópezOchoterena and Ochoa-Gasca 1971; Mayén-Estrada and Aladro-Lubel 1998, 2000,
2001, 2002, Vidal-Martínez et al. 2002)
, but there are no records from Chiapas state.
Epistylis hentscheli has been previously recorded as an ectoparasite of Cyprinus carpio
(Chordata, Cyprinidae) in Mexico (Herróz-Zamorano 1998), and
Zaleski and Claps
found this species on Enteromorpha sp. (Plantae, Chlorophyta) in Argentina.
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
and Chinchilla (1990)
who reported that the location of epibiont ciliates is determined
by the structural characteristics of the ciliates, and genera such as Zoothamnium,
Vorticella, and Epistylis, with long stalks, adhere to body regions exposed to water currents,
such as uropods and pereiopods.
Fernandez-Leborans and Gabilondo (2006)
et al. (1997)
also indicated that the adhesion site of the ciliates not only depends on the
epibionts, but also depends on a series of other characteristics such as the locomotion,
shape, molting period, sex, and the behavior of the crustacean.
Epibiosis is a facultative association, in which both participants gain advantages
but also have disadvantages from this interaction
. In this
case, the advantage for the epibiont E. hentscheli is some protection against
predators and a constant water flow providing food and oxygen. However, there are also
some associated disadvantages, for example: the exoskeleton is molted as the
crayfish grows, necessitating recolonization of the new exoskeleton by the ciliate epibiont
(Mayén-Estrada and Aladro-Lubel 2000; Fernandez-Leborans and Gabilondo 2006)
The advantages for the basibiont Procambarus (Austrocambarus) sp. include protection
against desiccation and harmful ultraviolet radiation (Wahl 2008), while disadvantages
include the alteration of the body surface and reduced efficiency of locomotion and
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.
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