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Detrimental effect of peritrich ciliates (Epistylis sp.) as epibionts on the survival of the copepod Acartia bifilosa/Aerjalalise Acartia bifilosa isenditel esinevate ripsloomadest epibiontide (Epistylis sp.) kahjustav moju.

INTRODUCTION

Epibiosis is a widespread relationship in aquatic environments often involving planktonic microcrustaceans as hosts and a variety of organisms as epibionts, including bacteria, algae, protozoans, or even small metazoans (e.g., Ho & Perkins, 1985; Fernandez-Leborans, 2004). Generally, epibiosis has been viewed as a commensal relationship. However, several studies have shown that epibionts affect their hosts in different ways. They influence feeding due to competition with the hosts (Kankaala & Eloranta, 1987), decrease reproduction (Willey et al., 1990; Threlkeld & Willey, 1993; Weissman et al., 1993), and increase susceptibility to predation, because swimming as well as escape movements are limited (Willey et al., 1990; Chiavelli et al., 1993; Weissman et al., 1993). The last two behavioural traits influence copepod abundance and therefore affect the prey field of planktivorous fish. Previous studies have verified host preference among epibionts in some cases (Green & Shiel, 2000; Gilbert & Schroder, 2003). In addition, epibionts often occur on planktonic crustaceans under eutrophic conditions, but no associations have been proven between epibiont prevalence on zooplankton and water quality (Manca et al., 1996).

Ciliate epibionts that infest planktonic crustaceans (Fernandez-Leborans & Tato-Porto, 2000) have also been found in the Baltic Sea (Hirche, 1974; Wiktor & Krajewska-Soltys, 1994). These studies describe temporal distribution of epibionts without any specific further research. A similar investigation was carried out by Utz & Coats (2005) where spatial and temporal patterns of epibiont distribution on copepod populations were studied. However, studies on the impact of epibionts on the survival of the hosts are very scarce (Kankaala & Eloranta, 1987; Xu & Burns, 1991) and there are no relevant studies in the NE part of the Baltic Sea.

The current paper partly aims to fulfill this gap of knowledge by studying the influence of peritrich ciliates as epibionts on mesozooplankton in the Gulf of Riga. In the present study the effect of peritrich ciliates, Epistylis sp., was experimentally studied on the survival of adult females and males of the copepod Acartia bifilosa. This species was chosen as an object of investigation because it is one of the two dominant copepods in the study area (Line & Sidrevics, 1995.

MATERIAL AND METHODS

The experiment was carried out in July 2004. Copepods for the experiment were collected from Parnu Bay (NE Gulf of Riga) at station KS (Fig. 1) by vertical hauls through the whole water column with a Juday net (mouth surface area 0.1 [m.sup.2], mesh size 90 [micro]m). Animals used in the experiment were kept in surface water from the sampling station and taken to the laboratory within 1 h.

Only adult stages of A. bifilosa males and females were carefully separated from other plankton and detrital material. They were placed into water taken from the sampling station and pre-filtered through a 50-gym mesh net. The animals were used in the experiment within 24 h. Males and females of A. bifilosa with epibionts were placed into culture plates, each single individual separately in 0.5 mL of filtered seawater. The same procedure was done with uninfected individuals who did not bear epibionts on their body. The temperature during the 6-day trial was 21 [+ or -] 1[degrees]C and the experiment was performed in natural light conditions. The water was not changed during the experiment. Animals were checked every 12 h (8 a.m. and 8 p.m.) and counted for the dead and live individuals for the survival times. The animals were considered dead when they showed no signs of movement. Altogether 242 A. bifilosa adult specimens were used in the experiment, which were divided into four groups: males and females with and without epibionts, respectively.

[FIGURE 1 OMITTED]

After the experiment, A. bifalosa mortality percentage was found in the six-day period, which was in turn divided into 12-h periods. In addition average survival times and descriptive statistics (standard error and 95% confidence interval) were calculated. ANOVA Single Factor analysis was done with Statistica 6.1 (Statsoft) to prove the effect of epibionts on A. bifilosa specimens.

RESULTS AND DISCUSSION

The experiment showed higher survival among females compared to males (ANOVA: F= 35.89, p < 0.05). Further, uninfested and infested females had significant differences in their mortality as individuals carrying Epistylis sp. died considerably earlier (ANOVA: F = 9.22, p < 0.05). In contrast to females, the mortality for uninfested and infested males did not exhibit any significant differences (ANOVA: F = 0.87, p > 0.05). For the males, the most profound difference occurred after 24 h from the beginning of the experiment, but no general dissimilarity was found like with the females (Fig. 2, Table 1).

[FIGURE 2 OMITTED]

Despite the limited effect of epibionts on male survival, the prevalence of epibionts has harmful effects on the animals even if it is not a direct action like with parasitic protozoans, but influences host indirectly. Hindering host's movements and competing for food (Kankaala & Eloranta, 1987) epibionts definitely shorten the life span of their host. These are probably the most influencing factors why the survival was lower among animals bearing epibionts in this experiment. It is likely that animals infested with epibionts are much more visible to predators and therefore easier to capture (Chiavelli et al., 1993).

In this study the examined A. bifilosa specimens were colonized by Epistylis sp. However, different epibionts can be found on copepods and it is likely that they might influence the survival of their hosts differently than Epistylis sp. as found in the current study. Vorticella spp. and Zoothamnium spp. have been found on copepods in the Gulf of Gdansk (Wiktor & Krajewska-Soltys, 1994) and from brackish water bays in the USA (Utz & Coats, 2005). In the SW part of the Baltic Sea also Myoschiston centropagidariim Precht was found (Hirche, 1974).

The epibiont prevalence has generally been observed at the time when the host species are very abundant and dominate in plankton communities (e.g., Hirche, 1974; Chiavelli et al., 1993). The same is valid for the current study: during the sampling time A. bifilosa was the dominating copepod in the NE Gulf of Riga. However, the dominating copepod in spring and early summer in this region is Eurytemora affinis (Simm & Ojaveer, 2000; Kotta et al., 2004). Because earlier studies indicate that different epibionts show different preference for various hosts (Green & Shiel, 2000; Gilbert & Schroder, 2003; Utz & Coats, 2005), studies with E. affinis would be essentially needed with the following two primary questions: (1) does E. affinis have different epibionts on its body than A. bifilosa, and (2) what are the sex-specific survival rates? This is also very important from the food-web and fisheries perspective as nauplu of E. affinis are the first and primary prey for fish larvae in this region--one of the most important fish spawning and young fish nursery areas in the NE Baltic Sea (Simm & Ojaveer, 2000; Kotta et al., 2004).

In general, A. bifilosa individuals die rather quickly and due to this fact, prolonged experiments are difficult to carry out with them. While epibiontic protozoans are mostly sessile, they may be occasionally free-swimming (Manca et al., 1996). Therefore, in the longer-lasting experiments, the count of the infested animals may actually increase because of being potentially infested by the free-swimming forms.

ACKNOWLEDGEMENTS

I would like to thank Mart Simm for his supervision and support throughout the study and comments on earlier versions of the manuscript. This study was financed, in part, from the Estonian Science Foundation grant No. 6751 and the Estonian Target Financing Programme No. 0182578s03.

Received 16 May 2006, in revised form 2 May 2007

REFERENCES

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Fernandez-Leborans, G. 2004. Protozoan epibionts on Mysis relicta Loven, 1862 (Crustacea, Mysidacea) from Lake Lusiai (Lithuania). Acta Zool. (Stockh.), 85, 101-112.

Fernandez-Leborans, G. & Tato-Porto, M. L. 2000. A review of the species of protozoan epibionts on crustaceans. I. Peritrich ciliates. Crustaceana, 73, 643-683.

Gilbert, J. J. & Schroder, T. 2003. The ciliate epibiont Epistylis pygmaeum: selection for zooplankton hosts, reproduction and effect on two rotifers. Freshwater Biol., 48, 878-893.

Green, J. D. & Shiel, R. J. 2000. Mobiline peritrich riders on Australian calanoid copepods. Hydrobiologia, 437, 203-212.

Hirche, H. J. 1974. Die Copepoden Eurytemora affinis Poppe and Acartia tonsa Dana and ihre Besiedlung durch Myoschiston centropagidarum PRECHT (Peritricha) in der Shiel. Kiel. Meeresf., 30, 43-64.

Ho, J. & Perkins, P. S. 1985. Symbionts of marine Copepoda: an overview. Bull. Mar. Sci., 37, 586-598.

Kankaala, P. & Eloranta, P. 1987. Epizoic ciliates (Ijorticella sp.) compete for food with their host Daphnia longispina in a small polyhumic lake. Oecologia, 73, 203-206.

Kotta, J., Simm, M., Kotta, L, Kanosina, L, Kallaste, K. & Raid, T. 2004. Factors controlling longterm changes of eutrophicated ecosystem of Parnu Bay, Gulf of Riga. Hydrobiologia, 514, 259-268.

Line, R. & Sidrevics, L. 1995. Zooplankton of the Gulf of Riga. In Ecosystem of the Gulf of Riga between 1920 and 1990 (Ojaveer, E., ed.), pp. 175-186. Estonian Academy Publishers, Tallinn.

Manca, M., Beltrami, M. & Sonvico, D. 1996. On the appearance of epibionts on the crustacean zooplankton of a large subalpine lake undergoing oligotrophication (L. Maggiore, Italy). Mem. Ist. Ital. Iarobiol., 54, 161-171.

Simm, M. & Ojaveer, E. 2000. Dynamics of copepods and fish larvae in Parnu Bay (NE part of the Gulf of Riga) in the spring-summer period. Proc. Estonian Acad. Sci. Biol. Ecol., 49, 317 326.

Threlkeld, S. T. & Willey, R. L. 1993. Colonization, interaction, and organization of cladoceran epibiont communities. Limnol. Oceanogr., 38, 584-591.

Utz, L. R. P. & Coats, D. W. 2005. Spatial and temporal patterns in the occurrence of peritrich ciliates as epibionts on calanoid copepods in the Chesapeake Bay, USA. J. Eukaryot. Microbiol., 52, 236-244.

Weissman, P., Lonsdale, D. J. & Yen, J. 1993. The effect of peritrich ciliates on the production of Acartia hudsonica in Long Island Sound. Limnol. Oceanogr., 38, 61322.

Wiktor, K. & Krajewska-Soltys, A. 1994. Occurrence of epizoic and parasitic protozoans on Calanoida in the Southern Baltic. Bull. Sea Fish. Inst., 132, 13-25.

Willey, R. L., Cantrell, P. A. & Threlkeld, S. T. 1990. Epibiotic euglenoid flagellates increase the susceptility of some zooplankton to fish predation. Limnol. Oceanogr., 35, 952-959.

Xu, Z. & Burns, C. W. 1991. Effects of the epizoic ciliate Epistylis daphinae, on growth, reproduction and mortality of Boeckella triarticulata (Thompson) (Copepoda: Calanoida). Hydrobiologia, 209, 183-189.

Marko Visse

Estonian Marine Institute, University of Tartu, Maealuse 10a, 12618 Tallinn, Estonia; marko.visse@mail.ee
Table 1. Descriptive statistics for average survival of Acartia
bifilosa with standard error (SE) and confidence intervals (CI)
in the experiment

 Survival, Count of
Acartia individuals h animals SE CI

Males uninfested 45.6 25 4.2 8.3
Males infested with epibiont 40.8 72 2.6 5.2
Females uninfested 78.6 56 3.5 6.9
Females infested with epibiont 64.7 89 2.9 5.7
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Author:Visse, Marko
Publication:Proceedings of the Estonian Academy of Sciences: Biology/Ecology
Date:Sep 1, 2007
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