Indian Journal of Geo-Marine Sciences Vol. 45(7), July 2016, pp. 920-925

Occurrence of epibionts in coastal waters of Tamilnadu

S. Vijayalakshmi, P. Murugesan, S. Muthuvelu & T. Balasubramanian* Centre of Advanced Study in Marine Biology, Faculty of Marine Sciences, Annamalai University, Parangipettai – 608 502, Tamilnadu, India *[E-mail: [email protected] ]

Received 21 December 2012; revised 31 January 2013

Present study provides the distributional records of genera of protozoan namely Epistylis, , Veginicola, Acineta and Tokophyra as epibionts got attached on the body surface of zooplankton such as Labidocera pectinata, Euterpina acutifrons, Pontella danae, Pontella securifer, Corycaus danae, Metis jousseaumei, Disticoulus minor, Lucifer hansei, Tortanus forcipes, Oithona rigida, O.brevicornis and Gastropod veliger collected from Tuticorin and Ennore coastal waters. Five genera of ciliates viz., three peritrichids and two suctorians, were identified and classified within the subclass Peritrichia: Epistylis Ehrenberg, 1830 (Epistylidae), Vaginicola Lamarck, 1816 (Vaginicolidae) and Vorticella Linnaeus, 1767 (Vorticellidae); and Suctoria: Acineta Ehrenberg, 1834 (Acinetidae) and Bütschli, 1889 (Tokophrydae). Data collected suggest that the epibiont attachment on may have a significant impact on the health of the fish population due to the substantial reduction in the population density of the copepods leading to food scarcity for the fish populations which directly depend on them.

[Keywords: Epibionts, zooplankton, gastropod veliger, Ennore coastal waters, ecological functions]

Introduction suctorians, peritrichs etc., were found colonizing Epibiosis is a non-symbiotic, zooplankton. Epibiont ciliates can live on facultative, and inter-specific association of two several metazoan , including cnidarians, organisms, wherein one organism lives on the ctenophores, rotifers, annelid worms, surface (epibiont) of another organism crustaceans, insect larvae, molluscs, fishes and (basibiont). “Epibionts’ includes organisms that, tadpoles5, 9-11. The associations may not be during the sessile phase of their life cycle are obligatory, and the epizoic communities are attached to the surface of a living substratum, generally characterized by a high number of while the basibionts lodge and constitute a species which may occupy very specialized support for the epibionts1. Epibiosis is beneficial niches12. Although most of these for epibiont protozoa, which can be transported protozoans are not harmful to their hosts, in to regions rich in food, competing2 or not with higher density they can interfere in mobility of their hosts3, and to much more oxygenated the host9, or cause stress, which makes the host sites4. Also, by being fixed on moving more susceptible to contaminants and possibly substrates, they can avoid predation by other natural stress such as food limitation13. zooplankton5. Kudo6 stated that the dislocation Copepods are the most abundant of the host increases the chances of survival of metazoans in oceanic ecosystems14. They epibionts due to the increased flow of water provide a link between primary producers containing food items and to the fact that (phytoplankton) and higher trophic levels epibionts are taken to sites with possibly more (whales15 birds16 and fishes17) they, thus, play an appropriate physical and chemical conditions. important role in aquatic ecosystems. Body Wahl7 opined that more intense water flow, in surface of crustaceans including copepods, act addition to ensuring a greater nutritional supply, as conducive environment for many groups of facilitates the dispersal of excreta, while the organisms, which include the so-called epibionts mobility of the epibionts facilitates their own (bacteria, algae, protozoa and various dispersion and improves the gene flow of their invertebrates) and got settled on the body populations. Lynn and Small8 reported five surface of other living organisms18, 19. Further, groups of protozoans namely Asostomatids, copepods serve as hosts for parasitic Protozoa, Chonotrichids, Suctorians, Peritrichs and Monogenea as well or even Isopoda20-24. Heterotrichs as an epibionts. Several species of Although a few fragmentary studies on protozoa belonging to the groups of flagellates, the occurrence of epibionts were made long VIJAYALAKSHMI et al., OCCURRENCE OF EPIBIONTS IN COASTAL WATERS 921

before in temperate waters, not much two parts namely prosome and urosome; of information on the colonization of zooplankton these prosome consists of head, thorax, antennae by epibionts in tropical and subtropical systems and the urosome consists of egg sac, caudal style is available. Lopez25 reported the occurrence of regions, etc., Epistylis sp. and Synedra sp. on the zooplankton Tuticorin (Lat 8°45’N; Long. 78°12’E), during an annual cycle in Tule Reservoir the capital town of southern district in (Venezuela) and they also found that cyclopoid Tamilnadu is an important industrial and copepods as the suitable substrate for Epistylis harbour place. Study location is quite close sp. Celia Olabarria26 reported the occurrence of very nearer to the harbour, where the shoreline epibiont molluscs on neogastropod shells in is sandy and strewn with dead coral fragments sandy bottom of Pacific coast of Mexico. and dead shells. Range of tide is extremely Skovgaard and Saiz27 studied on the seasonal weak with tidal amplitude of 0.16 m during neap occurrence of protistan parasites such as tide and 0.70 m at spring tide. Water currents and Blastodinium as epiobionts on in this area generated by the influence of the planktonic copepods. Unlike others, southwest and northeast monsoons and are of Maybruck and Rogerson28 reported the low velocity. A larger area of this littoral region occurrence of protozoan epiobionts on the prop is exposed during low tide and the intertidal flat. roots of mangrove species. Similarly, Walkusz and Rolbiecki29 reported the ciliate epibiont such as Paracineta sp. and Ellobiopsis parasites on the body surface of some taxa namely Calanus finmarchiaus and C. glacialis in the Kongsfjorden area. Tan30 studied the epibiont infestation on Horseshoe crab Tachypleus gigas at Pantai Balok in Peninsular Malaysia, where they have reported the occurrence of acorn barnacle Balanus, pedunculate barnacle Octolasmis, and conical slipper shells Calyptraea on the carapace of horseshoe crab. Similarly, the occurrence of an epibiont on copepod was reported in the Velacherry Lake, Chennai, India31. However, the occurrence of epibionts on zooplankton was not reported hitherto from the coastal waters of Tamilnadu,

South east coast of India. Therefore, the present Fig. 1- Map showing the sampling points ENN (ENNORE): study was made with a view to study the 0.5km from the shore; 2km from the shore and 5km from occurrence of epibionts on zooplankton in the the shoreTNH (Tuticorin New Harbour): 0.5km from the coastal waters of Tamilnadu. shore; 2km from the shore and 5km from the shore

Materials and Methods Ennore Port is located on the Coromandel Coast, about 24 km north of The zooplankton samples were th collected at seasonal intervals from Tuticorin Chennai Port Chennai. It is the 12 major port of (TNH 0.5Km and Ennore coastal waters during India. Ennore Port lies on the northeastern 2008 to 2011 from the surface waters by corner of the state of Tamil Nadu on a flat horizontal towing of plankton net (0.35 µm coastal plain known as the Eastern Coastal mouth diameter) made up of bolting silk (cloth Plains. Both the regions are port associated area No.10; mesh size 200 µm) for half an hour. with greater influence of urban and industrial These samples were preserved in 4% formalin32 wastes. for qualitative analysis. Three 1 mL aliquots from each sample were examined using Leica Results and Discussion stereoscope binocular microscope32, 33. Zooplankton examined showed the Copepods were identified up to species level34. presence of epibiont ciliates on their body. In the Epibionts were identified using the classical present study, 4 genera of ciliates, 3 peritrichids work of Lynn and Small35. For the sake of and 2 suctorians, were identified. The species convenience, the whole body was divided into 922 INDIAN J MAR SCI VOL 45, NO. 7 JULY 2016

identified in the present study are classified below: Subclass: Peritrichia Stein, 1859 Family Epistylidae Kahl, 1935 Epistylis Ehrenberg, 1830 Family Vaginicolidae De Fromentel, 1874 Vaginicola Lamarck, 1816 Family Vorticellidae Ehrenberg, 1838 Vorticella Linnaeus, 1767 Figure 8) Subclass: Suctoria Claparède and Lachmann, 1858 Family Acinetidae Stein, 1859 Acineta Ehrenberg, 1834 Fig. 3- Labidocera acuta with Acenita sp. Family Tokophrydae Bütschli Tokophrya Bütschli, 1889 Presently colonial peritrichous ciliates of the genera such as Epistylis, Vaginicola, Viorticella and Suctorians namely Acineta and Tokophyra were commonly observed as epibionts on the copepods and gastropod veliger in the coastal waters of Tamilnadu. Maximum number of epibionts was attached on the gastropod veliger (45 ind.−1) followed by adult calanoid copepod Lapidocera acuta (33 ind.−1). Similar levels of attachments were also observed in Cyclopoid copepods: Oithona rigida (24 Fig. 4 ind.−1), Oithona brevicornis (30 ind.−1), Corycaeus catus (16 ind.−1) and Harpacticoid copepod: Euterpinna acutiferons (10 ind.−1) and Metis jousseaumei (38 ind.−1) and Decapoda: Lucifer hanseni (9 ind.−1). Plankton, being the host for these epibionts, the percentage of infected organisms in the population depends on the host species, location and season. Among the five genera, the highest level of infestation was shown by Epistylis niagarae, which were attached to the entire body of the copepod hosts. This is in agreement with the findings of Xu and Burns36 Fig. 4 & 5- Oithona rigida and O. brevicorni with Epistylis 37 niagarae and Willey who reported similar level of infestation in the adult planktonic crustaceans.

Fig.6- Corycaeus catus with Tokophrya sp. Fig. 2- Gastropod veliger with Tokophyra sp. and Epistylis niagarae VIJAYALAKSHMI et al., OCCURRENCE OF EPIBIONTS IN COASTAL WATERS 923

Likewise, the greater epibiont burden was found in the copepods (Labidocera acuta), followed by cladocerans, gastropod (Veliger) and decapod. It seems that the infestation was associated with the available adhesion surface offered by each group (host size and available area). Similar pattern of occurrence was observed earlier by Görtz9 who found that the number of vorticellids per cladocerans changed according to length class, with more individuals adhering to larger than to smaller hosts. The

Fig. 7- Euterpinna acutiferons with Tokophyra sp. number of epibionts increased with the length of their host, with the largest copepods accommodating more than 200 tiny protozoans. According to Threlkeld1 there is a positive relationship between epibiont burden and body size of the planktonic organisms since larger organisms (i) are easier targets for epibionts to get passively and randomly dispersed, (ii) swim more rapidly and find more epibionts, (iii) can filter water and attract more epibionts, and (iv) can create greater hydrodynamic perturbations that attract mobile epibionts capable of detecting them. Various genera of ciliates including

Epistylis are commonly observed as epibionts Fig. 8- Lucifer hansei with Epistylis sp. can be solitary or colonial. Epibionts are seen to attach mostly on rear side of the copepod’s prosome. There were more than 24 and 30 individuals of Epistylis got settled respectively on the entire body surface of Oithona rigida and O. brevicorni. Another species of Peritrichs epibiont such as Vaginicola was detected on the cephalothorax of Distioculus minor; the infestation density and load was higher in the abdomen compared to antennae or swimming legs. However, the load was very low when compared to Epistylis sp. detected from other copepods. Similarly, the suctorian Acineta sp. was found to attach on the caudal setae of Labidocera acuta and the Tokophyra sp. got

Fig.9- Metis jousseaumei with Vaginicola sp. (Bars: 100 settled on the prosome of Euterpinna acutiferon µm) and gastropod veliger. Some epibionts were found on the The frequent occurrence of ciliate mouth appendages, and a very few on the epibionts observed in the present study might antennules (Oithona brevicornis) and swimming have been favored by the host behavior, such as legs (Tortannus forcipatus), which is in its preference to places abundant with food and consistent with the results of previous studies 38-40 their attempt to avert adverse environmental made elsewhere . Presence of lower colony conditions or fatal events such as the grazing of density of epibiont on antennae and swimming its surface by animals12. Epibiontic ciliates of legs suggested that these mobile parts become the Paracineta were found on the body harder to colonize than cephalothorax and surface of some copepod taxa collected in the abdomen. In the present study the Tokophrya sp. Kongsfjorden area (west Spitsbergen, Svalbard) got attached on the head of Corycaeus catus and during summer 2002. also the caudal region. This is in harmony with 924 INDIAN J MAR SCI VOL 45, NO. 7 JULY 2016

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