Epibiontic associations between apostomid ciliates Conidophrys spp. and amphipods associated with fish farms fouling in the western Mediterranean Sea
© The Author(s) 2016
Received: 10 November 2015
Accepted: 11 March 2016
Published: 1 December 2016
Fish farms commonly support high abundances of invertebrates, especially amphipods, associated with fouling communities developed over nets, ropes and buoys. Protozoan epibiont ciliates of the genus Conidophrys were observed on three of the most abundant amphipod species collected from ropes of a fish farm in the western Mediterranean Sea. The amphipod species were Ericthonius punctatus that presented the epibiont Conidophrys pitelkae, and Jassa marmorata and Jassa slatteryi with the epibiont C. pilisuctor. The epibionts were found in numbers fluctuating between 1 and 119 individuals in Jassa spp. (median value = 8), higher than the number of epibionts found on E. punctatus that varied between 1 and 39 individuals (median value = 3). The epibiosis on Jassa spp. also showed prevalence values (34.33 %) superior to those of E. punctatus (24 %). Differential distribution of the epibiont species on the surface of basibionts was detected: Conidophrys pilisuctor were more frequently found on the head and gnathopods of Jassa spp., while C. pitelkae were mainly counted on the head of E. punctatus. This is the first time that Conidoprhys were found on these amphipod species.
KeywordsProtozoa Pilisuctorids Marine habitats Jassa spp. Ericthonius punctatus
Epibiosis is a facultative association of two organisms: the epibiont and the basibiont. The term “epibiont” includes organisms that, during the sessile phase of their life cycle, are attached to the surface of a living substratum, while the basibiont lodges and constitutes support for the epibiont. Both concepts describe ecological functions [38, 41]. The surface of the basibiont usually is colonised by the epibiont because the need of hard substrate. This is especially important in areas where hard substrata are scarce—such as pelagic habitats—and epibiont species with sessile phases of their life-cycle can attach to the surfaces available like the exoskeleton of crustacea. Basibiont species may belong to different animal phyla: Bryozoa, Chaetognata, Cnidaria, Crustacea, Echinodermata, Enteropneusta, Insecta, Mollusca, Polychaeta, Porifera, Protozoa, Tunicata to Vertebrata [5, 35, 41]. Moreover, several crustacean groups also contain basibiont species: cladocerans, copepods, cirripedes, isopods, amphipods, and decapods . The epibiont species on crustacea can belong to Porifera, Cnidaria, Platyhelminthes, Nemertea, Rotifera, Nematoda, as well as Polychaeta, Cirripedia, Decapoda, Gastropoda, Bivalvia, Phoronida, Bryozoa and Ascidiacea . This association implies not only a protection and support for the epibiont, but also a great number of interactions (trophic, ecological, dispersive, etc.) and important effects on the partners of this relationship. In marine environments, epibiosis show a colonisation process that follows a series of consecutive phases, with a variety of organism groups involved. The area between epibiont and basibiont represent an interference mediation that can modify the effects not only on the organisms implicated, but also on the overall community . The organisms had evolved showing alterations in physiology and morphology adapted to this relationship. The synchronization of life-cycles as in the case Zoothamnium intermedium and copepods , indicates the way in which epibiont and basibiont species evolved, producing mobile phases before the moult of the basibiont. The specificity of epibionts is also important, indeed, there are epibiont groups found exclusively on crustacea, such as protozoan chonotrichids, and epibiont species that only live in a certain crustacean species . Among the ciliated protozoan epibionts on crustacea, one of the most specific groups is the apostomatid ciliates, including the order Pilisuctorida. The genus Conidophrys, belonging to this order, has been found on several crustacean species, mainly amphipods and isopods.
In the Mediterranean Sea, fish farms commonly support high abundances of invertebrates, especially amphipods, associated with fouling communities developed over nets, ropes and buoys. The cosmopolitan gammarids Ericthonius punctatus (Bate 1857), Jassa marmorata Holmes, 1905 and Jassa slatteryi Conlan, 1990 are frequently found in high abundances in these fouling habitats. Protozoan epibiont ciliates of the genus Conidophrys were observed on these three amphipod species collected from ropes of a fish farm in the western Mediterranean Sea. Accordingly, the aim of this work was to describe biological, biometric and taxonomical features of these epibionts in order to identify the Conidophrys species and to carry out a detailed study of their location on the body of Jassa spp. and E. punctatus to study whether the epibiont displays any preference for certain parts of the amphipods.
Amphipods, inhabiting fouling communities at a fish farm, were sampled by scraping fouling organisms from mooring ropes. The fish farm, dedicated to the on-growing of sea bream (Sparus aurata) and sea bass (Dicentrarchus labrax) were sampled off the coasts of Guardamar del Segura (Alicante, SE Spain: 38°5′45.88″N; 0°36′15.84″W) in June 2010. The samples were sieved through a 250 µm mesh with seawater and subsequently preserved in 4 % formalin. Individuals of J. marmorata, Jassa slatteryi and E. punctatus were sorted out and identified and numbers per sample were recorded. A total of 200 individuals of Jassa spp. and 150 of E. punctatus were revised for the presence of epibionts and examinations were subdivided into different body parts: Head, first and second antennae, buccal parts, first and second gnathopods, pereiopods, pleopods, uropods, pereion, pleon, urosome and telson. The ciliates were identified using an Image Analysis (Zeiss K 300) system with a Zeiss compound microscope. The measurements of ciliates were done using the computer program ScopePhoto 2.0. For slide preparations, the material was stained with Boehmer’s haematoxylin and mounted in Canada balsam. In order to identify the protozoan epibionts, they were isolated and treated using the silver carbonate technique, according to , and also with methyl green and neutral red.
For scanning electron microscopy, specimens of Jassa spp. were dehydrated in an ethanol series, critical point-dried in CO2 using a Polaron E3000, and sputter-coated in a Polaron SC500 using 60 % gold–palladium. Samples were then examined with a Philips XC30.
SEM operating at 15 kV. For transmission electron microscopy, Jassa spp. pereiopods were fixed in 3.0 % glutaraldehyde in 0.2 M sodium cacodylate buffer, pH 7.2 for 12 h at 48C, washed in the same buffer for 4 h at 48C and then postfixed in buffered 2.0 % osmium tetroxide for 4 h at the same temperature. After dehydration in a graded ethanol series, the pereiopods were embedded in Epon and sectioned with a diamond knife to identify the regions where the ciliates were attached to the pereiopod. Once located, ultrathin sections were prepared, double-stained with uranyl acetate and lead citrate, and observed in a JEOL 100CXII TEM operated at 80 kV. Statistical analyses (multiple-sample comparison and correlation analyses) were performed using the Statgraphics program.
The epibiont species
Phylum Intramacronucleata Lynn, 1996
Class Oligohymenophorea De Puytorac et al., 1974
Subclass Apostomatia Chatton & Lwoff, 1928
Order Pilisuctorida Jankowski, 1966
Family Conidophryidae Kirby, 1941
Genus Conidophrys Chatton & Lwoff, 1934
Conidophrys pilisuctor Chatton & Lwoff, 1934
Locality: Guardamar del Segura (Alicante)
Basibiont: On the amphipods J. marmorata Holmes, 1905 and Jassa slatteryi Conlan, 1990.
Biometrical measures of the epibiont species in the literature and in the present study
C. pitelkae (MEAL)
C. pitelkae (BT)
C. pilisuctor (MEAL)
C. pilisuctor (HR)
C. pilisuctor (CH)
Conidophrys (Jassa) (present study)
Trophotomont (1 tomite)
Trophotomont (2 tomites)
Conidophrys (Ericthonius) (present study)
Trophotomont (1 tomite)
Trophotomont (2 tomites)
Minimum and maximum values of number of epibionts (mean) on the different colonised anatomical units
Conidophrys pitelkae Bradbury, 1975
Locality: Guardamar del Segura (Alicante)
Basibiont: Ericthonius punctatus (Bate, 1857)
Description: Ciliates with a life cycle dimorphic and related to the moult cycle of the basibiont crustacean. There was a trophont, long, cylindrical, tapering slightly at the proximal end, covered by a cyst wall (Fig. 7). The cytostome contacted to the surface of the basibiont, the ciliate feeding on the secretions of the setae. The trophont becomes trophotomont (Figs. 8, 19, 20) when reproduced by tomitogenesis forming inside ciliated tomites. The tomites are finally released and may infest basibionts. When the tomite is attached to the host it becomes trophont . The macronucleus was serpentine or band shaped longitudinally crossing the body.
These suctorians were similar to those of C. pitelkae. “Trophont is elongate, slender cone shaped, and enclosed in a thin, transparent cyst. Trophont showed two fields of longitudinal unciliated kineties, a right with four and a left with six kineties. The macronucleus is long, serpentine, with conspicuous endosomes, fan-shaped at distal end. There is a micronucleus near the macronucleus. There is single contractile vacuole. Reproduction is by successive linear palintomy forming a single tomite. Tomite is a flattened with dorsal surface curved, with two large ventral depressions, anterior leads to cytostome. Five kineties form a ciliary fringe encircling partly the tomite lateral surface, whereas other five kineties form the ventral ciliature. Macronucleus of tomite is rod-shaped and oriented antero-posteriorly” . Biometrical data of the ciliates were similar to those of former description of C. pitelkae (Table 1). The key character of this species—a ribbon-like macronucleus with appreciable widening at the upper part of the cell body in tomont stages—was also observed in these ciliates .
Distribution: the epibionts were located on the surface of the body, mainly on the head and pereion, and less frequently on the pleon and urosome. It was also frequent on antennae. No epibionts were recorded on appendages (Table 2).
Spatial location of the epibiosis
Number of basibionts with and without epibionts, prevalence (%) and epibiosis intensity (mean number of Conidophrys per basibiont ± SE)
Jassa spp. (C. pilisuctor)
14 ± 3
E. punctatus (C. pitelkae)
6 ± 1
The relative proportions of the number of epibionts in different areas of the body considering the anterio-posterior axis of the basibiont of both amphipod species is shown in Fig. 2. There was a significant difference in the multiple sample comparison analysis (p < 0.05, n = 351) in the epibiosis prevalence between both amphipod genera. The correlation analysis carried out to test differences in the number of epibionts on the anatomical unit colonised between right and left sides of the amphipod indicated that in Jassa spp. all pereiopods and second and third uropods were significantly correlated, thus indicating a similar colonisation in right and left appendages (p < 0.05, n = 40), while in E. punctatus only correlated the fourth pereiopods (Table 2).
Jassa marmorata, J. slatteryi and E. punctatus are tubicolous marine amphipods belonging to Ischyroceridae family, which are widely distributed in fouling communities and hard substrata around the world [3, 36]. This study is the first describing the epibiont presence of apostomid ciliates Conidophrys spp. on these three species.
The most important difference between C. pilisuctor and C. pitelkae was referred to the stages of the trophont, from the settlement of the tomite on the surface of the basibiont. The epibionts of C. pilisuctor, observed on Jassa spp., presented stages of tomont, trophotomont, spheroid, lacrymoid and cucurbitoid. In contrast, the epibionts of C. pitelkae, recorded on E. punctatus, were smaller than those of C. pilisuctor and presented stages of tomont and trophotomont, all trophonts showing a similar morphology except for the size of the body.
The measures of C. pilisuctor on Jassa spp. were similar to those indicated by Mayén-Estrada and Aladro-Lubel  for Hyalella azteca. The measures of C. pitelkae on E. punctatus were similar to those of  for the shrimp Crangon crangon (Table 1).
With regard to the TEM images of the feeding complex of C. pilisuctor, there are several descriptions in the literature about this apparatus in apostomatids. In Conidophrys, the sole work was performed in C. pitelkae  describing its connection with the setae of the decapod C. crangon. Most of the organisms observed in this study were directly attached to the cuticle of the basibiont rather to their setae, and thus precludes direct comparison of their feeding complex. Analogies between both species are the tubules that constitute the cytostome running parallel to the surface of the cuticle, which provide the contact between epibiont and basibiont by fusion with the cuticle (Fig. 22b). Some of these tubules also pass through the cuticle into the lumen created between the cuticle layers of the basibiont. The ciliate structure found within the lumen of the amphipod (Fig. 21b) resembles the food tube described for Ascophrys sp. , but we did not find an extensive digestion of the cuticle of the basibiont as observed in the cuticle of Palaemon serratus. Comparatively, the feeding complex of C. pilisuctor was less complex and more superficial than those of C. pitelkae and Ascophrys sp. The images of the present study represent the first data about the feeding apparatus of C. pilisuctor.
Conidophrys species and their basibionts: isopod (I), amphipod (A), decapod (D), misidacean (M)
Jaera ischiosetosa (I)
South Wales, UK
Ilyarachna bergendali (I), I. hirticeps (I), I. torleivi (I), and Tytthocope megalura (I)
Idothea baltica (I)
Øresund (between Denmark and Sweden) and from Isefjord (Northern Sealand, Denmark)
Limnoria lignorum (I)
Hyalella azteca (A)
Pátzcuaro Lake (Michoacán Mexico)
Monocorophium acherusicum (A), Hyale perieri
M. acherusicum (A)
Mediterranean Sea near Set (France)
Gammarus locusta (A), G. oceanicus (A)
Øresund (between Denmark and Sweden) and from Isefjord (Northern Sealand, Denmark)
M. acherusicum (A)
M. acherusicum (A), Ericthonius difformis (A), Microdeutopus gryllotalpa (A), Jassa falcata (A), J. dentex (A), Gammarus locusta (A), Dexamine spinosa (A)
Melita petronioi (A)
Pombas Island, inside the Patos Lagoon, Rio Grande do Sulstate (Brazil)
Crangon crangon (D)
Atlantic coast of France
Penaeus setiferus (D)
Tamiahua lagoon (Atlantic coast of Mexico)
Mesopodopsis orientalis (M), Acetes japonicus (D), A. sibogae (D), A. indicus (D), Fenneropenaeus merguiensis (D)
Mangrove areas of Malaysia
Gammarus balcanicus (A)
Freshwater areas Ukraine
Sphaeroma serratum (I)
Jaera ischiosetosa (I)
South Wales, UK
Gammarus oceanicus (A)
G. subtipicus (A)
G. aequicauda (A)
Sivash Gulf of the Sea of Asov
G. olivii (A)
Bay, Black Sea
Conidophrys pilisuctor has been reported on isopods and amphipods. On the freshwater amphipod Hialella azteca, C. pilisuctor was found on pereiopods and antennae . Equally, on the isopod Idothea baltica and the amphipods Gammarus locusta and G. oceanicus, it was recorded on the setae of pereiopods . On the isopod Jaera albifrons on antennae, antennulae and pereiopods . On the isopod Limnoria lignorum and the amphipod Monocorophium acherusicum, it was found on “secretory hairs” of the cuticle . Finally, it was mainly reported on gnathopods, pereiopods, and less abundantly on pleopods and uropods of the amphipod Melita petronioi .
From these studies, the distribution of Conidophrys on the different basibiont species varied significantly, although it seems that there was a preference for the setae of the cuticle, and the appendages of the anterior half of the body. In our study the epibionts were mainly present directly on the cuticle of the amphipod and to a lesser extent on the setae of their pereiopods. However, there are some findings when the host setae were short that created the illusion of a direct attachment to the hosts’ cuticle. For example according to  the attachment to the short setae observed in C. pilisuctor in particular from the amphipod crustacean Jassa falcata. The three studied amphipods, J. marmorata, J. slatteryi and E. punctatus produce ‘amphipod silk’, through specialized glands in the third and fourth pereiopods, and build tubes cemented with fine suspended matter where they live . Inside them, they protrude water movements to filter organic matter and gather detritus  that may be related to the greater probability of becoming colonised on the anterior part. Thus, the production of amphipod silk could be also related to the higher colonisation of the third and fourth pereiopods. Moreover, this rich environment of external nutrients may be responsible to the higher distribution of the epibionts directly on the cuticula than on the setae of the amphipods .
Conidophrys has its entire life-cycle on the crustacean basibiont. There is a synchronization between the life-cycles of epibiont and basibiont, where the premoult events of the crustacean determine the tomitogenesis in Conidophrys trophont, so that the tomites are released in the water environment when moulting occurs. Tomites can colonise new surfaces, including the new cuticle of the basibiont . The epibiont contacts with the basibiont by means of the cytostome, and exudate secretions from the basibiont cuticle—i.e. hemolymph—are incorporated through the cytostome into the cytoplasm of the ciliate. Therefore, the impact of the epibiont on the external surface of the crustacean, from the feeding point of view, depends on the abundance of trophont stages on the cuticle of the basibiont.
The prevalence on Jassa spp. was 34.33 % and on E. punctatus 24 %. In H. azteca, these percentages for C. pilisuctor fluctuated between 23.4 and 55.2 % . On that study the high values of number of epibionts were recorded on the pereiopods and the antennae, while in the individuals of Jassa spp. the highest numbers of epibionts were observed on the head, second gnathopods, and third and fourth pereiopods. Regarding C. pitelkae, the highest percentages of this ciliate on Penaeus setiferus were observed on the pereiopods and pleopods , while on E. punctatus, the epibionts were more abundant on the surface of the head and pereion. This fact may indicate that the preference of epibionts for certain body parts might vary according to the crustacean basibiont species, their biological activities and the characteristics of their cuticle. The fact that all amphipods studied herein are tube-building could facilitate the settlement of tomites, preventing them from being dragged by the currents.
Epibiosis does not imply to fill certain requirements for the participants, except for attachment to a substrate. There could be indeed a number of effects on both the epibiont and the basibiont, and the relation could be considered from symbiosis to commensalism and parasitism. The epibiosis might produce evolutive changes in the participants in the long term [1, 29]. The effects can be advantages for the epibiont in dispersal and geographical expansion, increasing the supply of nutrients and protection against predation or negative condition of the environment . Epibiosis can be disadvantageous for the epibiont by causing ontogenetic or behavioural changes on the basibiont . Epibiosis can be beneficial for the basibiont by providing both mimetic protection and cleaning [18, 25]. On the contrary, epibiosis may be negative for the basibiont by restricting mobility and affect growth, moulting and functionality of several organs (eyes, gills and appendages), causing an increase in predation hazard. Epibiont and basibiont might compete for nutrients . In the case of the epibiosis of the present study, several areas of the basibiont, such as the head and anterior appendages (gnathopods and pereiopods), showed a relatively high number of epibionts, and this fact could have negative effects on the sensorial activity of the crustacean. In addition, the epibionts on the surface of the appendages may restrict the ability of movement.
Also, certain tube-building amphipod species such as Crassicorophium bonellii and Lembos websteri ingest tube-wall material during poor feeding conditions, especially around the tube entrances . This fact might negatively affect the epibiont populations, since epibionts were not protect and may be eliminated due the grooming and cleaning or other antifouling activities of the amphipod. In the other sense, the contribution of tubicolous amphipods to biofouling is important, and they achieve improved natural dispersal ability, being this fact reflected on the present epibiontic species .
The high densities of the two Jassa species and E. punctatus associated to the fish farm fouling (Fernandez-Gonzalez, pers. obs) may increase the release of tomites to the marine environment and also ensure the availability? of basibiont individuals around them. Moreover, the water around the fish farm is extremely rich in organic substances  that can favour the development of the ciliates. This leads to raise the following hypotheses: (1) that free-living amphipods—planktonic or benthic not tube-building—would be less susceptible to this type of epibiosis, (2) tube amphipods of control areas—with a lower input of organic substances—would have less ciliates than those close to the fish farm. Overall, this study reveals the presence of two apostomatid ciliate epibionts in three tube-building amphipods around fish farms and their spatial distribution around the body of the basibionts. More studies need to be done to address the former hypotheses in order to know if the rich-nutrient environment around the fish farms might benefit the ciliate epibiosis.
GFL participated in the samples observation, epibiont identification. VFG participated in sampling, identification of basibionts, and measurement of paremeters involved in the epibiosis. PSJ participated in sampling. AR participate in obtention of SEM images of the epibiont and schemes of the organisms. All authors contributed in drafted the manuscript. All authors read and approved the final manuscript.
The authors thank Inés Pazos and Jesús Méndez (CACTI, University of Vigo) (IIM, Vigo) for their technical support preparing the samples for electron microscopy. We are indebted to Santiago Pascual (IIM, CSIC) for supporting the electron microscopy carried in this study. AR is supported by a “Fundación Barrié de la Maza” postdoctoral fellowship and a Securing Food, Water and the Environment Research Focus Area grant (La Trobe University).
The authors declare that they have no competing interests.
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