Gasterosteus Aculeatus) Infection with Schistocephalus Solidus in Hel Marina (Puck Bay, Baltic Sea, Poland) by Abstract
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Oceanological and Hydrobiological Studies International Journal of Oceanography and Hydrobiology Volume 44, Issue 1, March 2015 ISSN 1730-413X pages (11-17) eISSN 1897-3191 The three-spined stickleback (Gasterosteus aculeatus) infection with Schistocephalus solidus in Hel marina (Puck Bay, Baltic Sea, Poland) by Abstract Zdeněk Mačát* Parasitic relations between animals are very common in wild nature. In this paper, we studied levels of infection in Adam Bednařík three-spined stickleback with plerocercoids of Schistocephalus Martin Rulík solidus from Puck Bay (Baltic Sea, Poland). The total prevalence of infection was 54.2%, while proportion of infected individuals was significantly higher for females than for males. The body width was found to be significantly positively correlated with the number and the weight of parasites. In spite of the increasing deterioration of the Baltic Sea ecosystem by excessive eutrophication and hypoxia, lower DOI: 10.1515/ohs-2015-0002 prevalence of infection compared to previous published data Category: Original research paper indicates that there are likely other factors than pollution affecting the life cycle of parasites and the level of parasitism. Received: November 7, 2014 Accepted: December 11, 2014 Department of Ecology and Environmental Sciences, Faculty of Science, Palacký University, Šlechtitelů 11, 783 71 Olomouc, Czech Republic Key words: parasite, infection prevalence, Schisto- cephalus solidus, three-spined stickleback, Puck Bay * Corresponding author: [email protected] The Oceanological and Hydrobiological Studies is online at oandhs.ocean.ug.edu.pl ©Faculty of Oceanography and Geography, University of Gdańsk, Poland. All rights reserved. 12 Oceanological and Hydrobiological Studies, VOL. 44, ISSUE 1 | MARCH 2015 Zdeněk Mačát, Adam Bednařík, Martin Rulík Introduction 1976). It is an anadromous species with numerous resident populations in brackish or pure freshwater, Parasitism is one of the most common rarely in sea waters (Wooton 1976, NatureServe relationships between organisms. It may have an 2013). Sticklebacks are common fish species in impact on phenotypes, ecology and evolution of a the Baltic littoral zone (Morozińska-Gogol 2011); host. Phenotypic changes can also mean changes two from three main lateral plate morphs most in morphology, physiology and behavior (Poulin frequently occur in the Gulf of Gdańsk: trachurus & Thomas 1999, Moore 2002, Dingemanse et al. and semiarmatus, while the leiurus morph is rare or 2009). Plerocercoids of Schistocephalus solidus missing (Bańbura 1994, Morozińska-Gogol 2011). (Müller, 1776) are common parasites of three-spined Numerous parasitological studies have focused sticklebacks Gasterosteus aculeatus Linnaeus, 1758 on sticklebacks as they are suitable study objects; (hereafter referred to as stickleback) in fresh and they often occur at high population densities, are brackish waters in the whole range of the fish (Barber easy to catch and have a widespread, circumpolar & Scharsack 2010). distribution (e.g. Lobue & Bell 1993, Tierney 1994, S. solidus is a trophically transmitted Barber & Huntingford 1995, Ranta 1995, Ness pseudophyllidean cestode with a three-host life & Foster 1999, Poulin et al. 2011, Hendry et al. cycle that uses the stickleback as its intermediate 2013). Sticklebacks are also popular model hosts host (Chubb et al. 2009, Barber & Scharsack 2010). in ecological and evolutionary parasitology for Eggs of S. solidus hatch in freshwater and the free- several reasons (e.g. Heins & Baker 2008, Barber & swimming coracidium is ingested by various Scharsack 2010, Barber 2013). However, permanent copepods. The procercoid grows in the haemocoel degradation of water environment is observed due of the copepod and, after 10-11 days of infection, it to various kinds of anthropogenic impact. This may is able to establish through ingestion by its second affect the abundance of parasitism cases (Mackenzie intermediate host (Chubb et al. 2009). Sticklebacks et al. 1999, Lafferty, 1997, Sures 2004, Marcogliese acquire infections when they feed on parasitized 2005). With respect to this fact, it is necessary to copepods, and infective procercoids shed their outer have long term data about trends of prevalence and layer together with the cercomer in the stickleback intensity of infection. A typical example of depleted digestive tract, and then penetrate the wall of areas is the Baltic Sea, which in recent years suffers the intestine. The parasite then develops into a particularly from excessive eutrophication (Kautsky plerocercoid, which grows to a large size in the fish et al. 1986, Rönnberg & Bonsdorff 2004), hypoxia host’s body cavity. The life cycle is completed when (Conley 2012; Carstensen et al. 2014a,b) and invasion sticklebacks harboring infective plerocercoids are by alien species (Leppäkoski & Olenin 2000, Paavola ingested by a definitive host (Clarke 1954, Barber et al. 2005, Ojaveer & Kotta 2006). & Scharsack 2010). The definitive host can be any This study is based on samples of stickleback warm-blooded vertebrate; most typically these collected during the stay at the Hel Marine Station are fish-eating birds (Giles 1983) though other of the University of Gdańsk, the Institute of endotherms can harbor adult worms (Hoberg et al. Oceanography. Our objective was to assess the 1997). level of prevalence of S. solidus in sticklebacks and Sticklebacks are native species with a wide compare our results to other data available from the distribution and a large number of subpopulations. Baltic Sea and elsewhere. The occurrence of this species includes the coastal waters of Eurasia, Iceland, eastern Asia and Materials and methods Northern America (Wooton 1976, NatureServe 2013). Sticklebacks are typically found in quiet The sticklebacks were collected with a small weedy pools and backwaters. They are also found seine net operated by two persons and a plankton in the marginal vegetation of streams, over sand net in Puck Bay, near the Hel Marina (54°36’31”N; and mud bottom substrates. Marine populations 18°47’44”E) and the adjacent shallow sandy coast in are pelagic and usually found inshore along the June and July 2013. Puck Bay is a shallow western coast, in estuaries and coastal lagoons (Wooton branch of the Gulf of Gdańsk in the southern Baltic www.oandhs.ocean.ug.edu.pl ©Faculty of Oceanography and Geography, University of Gdańsk, Poland. All rights reserved. Oceanological and Hydrobiological Studies, VOL. 44, ISSUE 1 | MARCH 2015 13 The three-spined stickleback infection with Schistocephalus solidus Sea and its salinity is in the range of 6-8 PSU. All Results fish caught were immediately fixed in ethanol (70%). The weight, the maximum length and the width of Altogether 94 individuals (33 males and 61 fish were measured in a laboratory (Ohaus LS 2000 females; 61 trachurus, 29 semiarmatus and 4 leirus) electronic weighing scales with an accuracy of 0.1 of three-spined stickleback were caught. The fish g and dial callipers with an accuracy of 0.1 mm) varied significantly in their size (body length; range for each specimen, and the occurrence of possible 42.2-69.6 mm; mean ± SD = 53.0 ± 4.2 mm). The ectoparasites were checked. A photograph of each weight of parasites ranged from 0.31g to 0.99 g; fish was also taken for a precise identification of the mean ± SD = 0.50 ± 0.14 g, N = 58 individuals. The lateral plate morph. Specimens of stickleback were proportion of infected individuals was significantly dissected to remove S. solidus plerocercoids and to higher for females (65.6%; intensity 0.73) compared determine their sex. to males (33.3%; intensity 0.39) (p < 0.05), while no Prevalence with plerocercoids of S. solidus, the significant difference was found for three examined mean and the range of infection intensity were morphotypes. Total prevalence of infection by calculated according to Bush et al. (1997) and Rózsa Schistocephalus plerocercoids was 54.2% (51 out of et al. (2000). Prevalence (%) is the proportion of 94 fish), while the intensity reached 1.1 (individual infected hosts among all hosts examined. Mean range 1-2). Data for individual morphs are also intensity is the arithmetic mean of the number presented (Table 1). of individuals of a particular parasite species per Analysis of the relationship between the different infected host in a sample. Intensity range is the parameters (body length, width, weight) and the highest and lowest number of individuals of a number of parasites by ANOVA and the multiple particular parasite per infected host in a sample. regression method revealed that the body width was These measures of infection were calculated for significantly positively correlated with the number the entire stickleback sample and also for lateral and the weight of parasites (r2 = 0.41; r = 0.64; p < plate morphotypes trachurus and semiarmatus 0.05; Fig. 1). because the leirus morph occurred only once in our sample. The morphs were determined on the basis of Bańbura (1994). Discussion Data analyses were performed by using the software STATISTICA 12 (StatSoft 2013). Sample The cestodan S. solidus is considered to be a differences were statistically compared using limnetic species (Zander 1998). It occurs in several one-way analysis of variance and independent birds as final hosts which prey on the stickleback; two-sample t-test (P < 0.05). To investigate the this fish is the solely second intermediate host in relationships between variables, multiple regression fresh waters. However, S. solidus can infect also fish analysis of data was performed. species of marine origin like gobies and cod (e.g. Zander & Kesting 1996). It has also been found in the Table 1 Values of infection prevalence and intensity for each morph, compared to data from this research morph trachurus semiarmatus leiurus total prevalence intensity prevalence intensity prevalence intensity prevalence intensity year (%) (ind.) (%) (ind.) (%) (ind.) (%) (ind.) 1.2 1.1 1.2 1.2 1994* 4.6 8.5 10.6 5.0 (1-2) (1-2) (1-3) (1-3) 1.8 3.0 2.2 2008* 91.7 100 n.c. n.c. 94.4 (1-4) (1-6) (1-6) 1.2 1.1 1 1.1 2013 49.2 65.5 50.0 54.2 (1-2) (1-2) (1) (1-2) * - observed by Morozińska-Gogol (2011); n.c.