The three-spined stickleback (Gasterosteus aculeatus) infection with Schistocephalus solidus in Hel marina (Puck Bay, Baltic Sea, Poland)

Abstract

Parasitic relations between animals are very common in wild nature. In this paper, we studied levels of infection in three-spined stickleback with plerocercoids of Schistocephalus 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 prevalence of infection compared to previous published data indicates that there are likely other factors than pollution affecting the life cycle of parasites and the level of parasitism.

Full text

Oceanological and Hydrobiological Studies
International Journal of Oceanography and Hydrobiology
Department of Ecology and Environmental
Sciences, Faculty of Science, Palacký University,
Šlechtitelů 11, 783 71 Olomouc,
Czech Republic
Volume 44, Issue 1, March 2015
ISSN 1730-413X
eISSN 1897-3191
* Corresponding author: zdenek.macat@gmail.com
©Faculty of Oceanography and Geography, University of Gdańsk, Poland. All rights reserved.
DOI: 10.1515/ohs-2015-0002
Category: Original research paper
Received: November 7, 2014
Accepted: December 11, 2014
e three-spined stickleback (Gasterosteus aculeatus) infection with
Schistocephalus solidus in Hel marina (Puck Bay, Baltic Sea, Poland)
Zdeněk Mačát*
Adam Bednařík
Martin Rulík
by
The Oceanological and Hydrobiological Studies is online at oandhs.ocean.ug.edu.pl
pages (11-17)
Abstract
Parasitic relations between animals are very common in
wild nature. In this paper, we studied levels of infection in
three-spined stickleback with plerocercoids of Schistocephalus
solidus from Puck Bay (Baltic Sea, Poland). e total
prevalence of infection was 54.2%, while proportion of
infected individuals was signicantly higher for females
than for males. e body width was found to be signicantly
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
prevalence of infection compared to previous published data
indicates that there are likely other factors than pollution
aecting the life cycle of parasites and the level of parasitism.
Key words: parasite, infection prevalence, Schisto-
cephalus solidus, three-spined stickleback, Puck Bay
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Zdeněk Mačát, Adam Bednařík, Martin Rulík
www.oandhs.ocean.ug.edu.pl
Oceanological and Hydrobiological Studies, VOL. 44, ISSUE 1 | MA RCH 2015
©Faculty of Oceanography and Geography, University of Gdańsk, Poland. All rights reserved.
Introduction
Parasitism is one of the most common
relationships between organisms. It may have an
impact on phenotypes, ecology and evolution of a
host. Phenotypic changes can also mean changes
in morphology, physiology and behavior (Poulin
& omas 1999, Moore 2002, Dingemanse et al.
2009). Plerocercoids of Schistocephalus solidus
(Müller, 1776) are common parasites of three-spined
sticklebacks Gasterosteus aculeatus Linnaeus, 1758
(hereaer referred to as stickleback) in fresh and
brackish waters in the whole range of the sh (Barber
& Scharsack 2010).
S. solidus is a trophically transmitted
pseudophyllidean cestode with a three-host life
cycle that uses the stickleback as its intermediate
host (Chubb et al. 2009, Barber & Scharsack 2010).
Eggs of S. solidus hatch in freshwater and the free-
swimming coracidium is ingested by various
copepods. e procercoid grows in the haemocoel
of the copepod and, aer 10-11 days of infection, it
is able to establish through ingestion by its second
intermediate host (Chubb et al. 2009). Sticklebacks
acquire infections when they feed on parasitized
copepods, and infective procercoids shed their outer
layer together with the cercomer in the stickleback
digestive tract, and then penetrate the wall of
the intestine. e parasite then develops into a
plerocercoid, which grows to a large size in the sh
host’s body cavity. e life cycle is completed when
sticklebacks harboring infective plerocercoids are
ingested by a denitive host (Clarke 1954, Barber
& Scharsack 2010). e denitive host can be any
warm-blooded vertebrate; most typically these
are sh-eating birds (Giles 1983) though other
endotherms can harbor adult worms (Hoberg et al.
1997).
Sticklebacks are native species with a wide
distribution and a large number of subpopulations.
e occurrence of this species includes the coastal
waters of Eurasia, Iceland, eastern Asia and
Northern America (Wooton 1976, NatureServe
2013). Sticklebacks are typically found in quiet
weedy pools and backwaters. ey are also found
in the marginal vegetation of streams, over sand
and mud bottom substrates. Marine populations
are pelagic and usually found inshore along the
coast, in estuaries and coastal lagoons (Wooton
1976). It is an anadromous species with numerous
resident populations in brackish or pure freshwater,
rarely in sea waters (Wooton 1976, NatureServe
2013). Sticklebacks are common sh species in
the Baltic littoral zone (Morozińska-Gogol 2011);
two from three main lateral plate morphs most
frequently occur in the Gulf of Gdańsk: trachurus
and semiarmatus, while the leiurus morph is rare or
missing (Bańbura 1994, Morozińska-Gogol 2011).
Numerous parasitological studies have focused
on sticklebacks as they are suitable study objects;
they oen occur at high population densities, are
easy to catch and have a widespread, circumpolar
distribution (e.g. Lobue & Bell 1993, Tierney 1994,
Barber & Huntingford 1995, Ranta 1995, Ness
& Foster 1999, Poulin et al. 2011, Hendry et al.
2013). Sticklebacks are also popular model hosts
in ecological and evolutionary parasitology for
several reasons (e.g. Heins & Baker 2008, Barber &
Scharsack 2010, Barber 2013). However, permanent
degradation of water environment is observed due
to various kinds of anthropogenic impact. is may
aect the abundance of parasitism cases (Mackenzie
et al. 1999, Laerty, 1997, Sures 2004, Marcogliese
2005). With respect to this fact, it is necessary to
have long term data about trends of prevalence and
intensity of infection. A typical example of depleted
areas is the Baltic Sea, which in recent years suers
particularly from excessive eutrophication (Kautsky
et al. 1986, Rönnberg & Bonsdor 2004), hypoxia
(Conley 2012; Carstensen et al. 2014a,b) and invasion
by alien species (Leppäkoski & Olenin 2000, Paavola
et al. 2005, Ojaveer & Kotta 2006).
is study is based on samples of stickleback
collected during the stay at the Hel Marine Station
of the University of Gdańsk, the Institute of
Oceanography. Our objective was to assess the
level of prevalence of S. solidus in sticklebacks and
compare our results to other data available from the
Baltic Sea and elsewhere.
Materials and methods
e sticklebacks were collected with a small
seine net operated by two persons and a plankton
net in Puck Bay, near the Hel Marina (54°36’31”N;
18°47’44”E) and the adjacent shallow sandy coast in
June and July 2013. Puck Bay is a shallow western
branch of the Gulf of Gdańsk in the southern Baltic
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The three-spined stickleback infection with Schistocephalus solidus
Oceanological and Hydrobiological Studies, VOL. 44, ISSUE 1 | MA RCH 2015
©Faculty of Oceanography and Geography, University of Gdańsk, Poland. All rights reserved.
Sea and its salinity is in the range of 6-8 PSU. All
sh caught were immediately xed in ethanol (70%).
e weight, the maximum length and the width of
sh were measured in a laboratory (Ohaus LS 2000
electronic weighing scales with an accuracy of 0.1
g and dial callipers with an accuracy of 0.1 mm)
for each specimen, and the occurrence of possible
ectoparasites were checked. A photograph of each
sh was also taken for a precise identication of the
lateral plate morph. Specimens of stickleback were
dissected to remove S. solidus plerocercoids and to
determine their sex.
Prevalence with plerocercoids of S. solidus, the
mean and the range of infection intensity were
calculated according to Bush et al. (1997) and Rózsa
et al. (2000). Prevalence (%) is the proportion of
infected hosts among all hosts examined. Mean
intensity is the arithmetic mean of the number
of individuals of a particular parasite species per
infected host in a sample. Intensity range is the
highest and lowest number of individuals of a
particular parasite per infected host in a sample.
ese measures of infection were calculated for
the entire stickleback sample and also for lateral
plate morphotypes trachurus and semiarmatus
because the leirus morph occurred only once in our
sample. e morphs were determined on the basis of
Bańbura (1994).
Data analyses were performed by using the
soware STATISTICA 12 (StatSo 2013). Sample
dierences were statistically compared using
one-way analysis of variance and independent
two-sample t-test (P < 0.05). To investigate the
relationships between variables, multiple regression
analysis of data was performed.
Results
Altogether 94 individuals (33 males and 61
females; 61 trachurus, 29 semiarmatus and 4 leirus)
of three-spined stickleback were caught. e sh
varied signicantly in their size (body length; range
42.2-69.6 mm; mean ± SD = 53.0 ± 4.2 mm). e
weight of parasites ranged from 0.31g to 0.99 g;
mean ± SD = 0.50 ± 0.14 g, N = 58 individuals. e
proportion of infected individuals was signicantly
higher for females (65.6%; intensity 0.73) compared
to males (33.3%; intensity 0.39) (p < 0.05), while no
signicant dierence was found for three examined
morphotypes. Total prevalence of infection by
Schistocephalus plerocercoids was 54.2% (51 out of
94 sh), while the intensity reached 1.1 (individual
range 1-2). Data for individual morphs are also
presented (Table 1).
Analysis of the relationship between the dierent
parameters (body length, width, weight) and the
number of parasites by ANOVA and the multiple
regression method revealed that the body width was
signicantly positively correlated with the number
and the weight of parasites (r2 = 0.41; r = 0.64; p <
0.05; Fig. 1).
Discussion
e cestodan S. solidus is considered to be a
limnetic species (Zander 1998). It occurs in several
birds as nal hosts which prey on the stickleback;
this sh is the solely second intermediate host in
fresh waters. However, S. solidus can infect also sh
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
year prevalence
(%)
intensity
(ind.)
prevalence
(%)
intensity
(ind.)
prevalence
(%)
intensity
(ind.)
prevalence
(%)
intensity
(ind.)
1994* 4.6 1.2
(1-2) 8.5 1.1
(1-2) 10.6 1.2
(1-3) 5.0 1.2
(1-3)
2008* 91.7 1.8
(1-4) 100 3.0
(1-6) n.c. n.c. 94.4 2.2
(1-6)
2013 49.2 1.2
(1-2) 65.5 1.1
(1-2) 50.0 1
(1) 54.2 1.1
(1-2)
* - observed by Morozińska-Gogol (2011);
n.c. - morph was not caught in 2008
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14
Zdeněk Mačát, Adam Bednařík, Martin Rulík
www.oandhs.ocean.ug.edu.pl
Oceanological and Hydrobiological Studies, VOL. 44, ISSUE 1 | MA RCH 2015
©Faculty of Oceanography and Geography, University of Gdańsk, Poland. All rights reserved.
western parts of the Baltic Sea where it dominates
in gobiid shes (Zander et al. 1993). A number of
studies have examined S. solidus in fection preva lence
and intensity in natural stickleback populations,
and the phenotype (including appearance, energetic
condition, reproductive capacity and behavior)
of naturally infected sticklebacks has been well
documented. e proportion of sh harboring
infections can be extremely high, in some cases
approaching 100% (Hopkins & Smyth 1951), but this
varies considerably between populations (MacColl
2009), and temporally within a population (Chappell
1969).
Our results on the prevalence are less comparable
to data reported by Morozińska-Gogol (2011). She
studied prevalence of S. solidus in sticklebacks from
the Gulf of Gdańsk in 1994 when infection was
relatively low (5%), while in 2008, the level of infect ion
signicantly increased (94.4%). Rolbiecki et al. (1999)
found similar prevalence (6.3%) from the same area.
Freshwater species, like S. solidus, have better living
conditions in less saline water, thus we could expect
that sticklebacks from more saline water would
have lower prevalence of parasites compared to
freshwater localities. Indeed, Bergersen (1996) found
from 18 to 92% infected stickleback in freshwater
localities in Greenland, and Wootton (1976) − up to
88% in the United Kingdom. In addition, Valtonen
et al. (2001) reported the maximum prevalence of
45.6% for sticklebacks from the NE Bothnian Bay
where salinity values decrease to a freshwater level.
On the other hand, very low prevalence (3-14%) was
found in G. aculeatus from Mecklenburg Bight with
the salinity of 10-12 PSU (Zander & Reimer 2002,
Zander 2007). Extremely low prevalence was found
in resident and anadromous sticklebacks from Mud
Lake, Alaska (1.8% and 14%, respectively; Confer et
al. 2012).
Dierences in the prevalence and infectivity
based on the sex and ecology of sticklebacks have
been previously documented (Reimchen & Nosil
2001, Jäger & Schørring 2006, MacColl 2009). In
our samples, the prevalence of plerocercoids was
signicantly higher in females (65.6%) compared
to males (33.3%). However, Confer et al. (2012)
reported opposite ndings. It is still unclear why
Fig. 1.
Relationship between body width (blue rhombus) and body weight (yellow triangle) and weight of all specimens of
S. solidus per infected host in a sample
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15
The three-spined stickleback infection with Schistocephalus solidus
Oceanological and Hydrobiological Studies, VOL. 44, ISSUE 1 | MA RCH 2015
©Faculty of Oceanography and Geography, University of Gdańsk, Poland. All rights reserved.
the prevalence of plerocercoids was signicantly
higher in males than in females in the anadromous
population, but the authors suggest that the female
reproductive ability may be more aected than that
of males in an anadromous stickleback, resulting in
infected females disproportionally failing to return
to freshwater to breed.
Generally, parasite infections may aect host
phenotypic characteristics, including morphology
(Poulin & omas 1999). Dingemanse et al. (2009)
reported that the total parasite mass is related to
dierences in the trunk shape and head morphology
of stickleback. We also nd that intensity of
stickleback infection is associated with some
morphological changes (sh body width increases
with heavier total parasite mass).
e brackish conditions of the Baltic Sea is oen
claimed to be an obvious stress for all organisms,
including parasites. Generally, parasites depend on
the salt tolerance of their hosts, the most restricted
ones conne to the distribution of parasites.
For example, the population of eelpout Zoarces
viviparous (Linnaeus, 1758) has the most marine
parasite species in Lübeck Bight (salinity ca. 13 PSU),
while the most freshwater species associated with
this sh was found in more brackish water of the
Gulf of Gdańsk (salinity 7 PSU; Zander & Reimer
2002). However, the total number of parasites might
have been almost the same for both locations.
In our samples, the ectoparasitic copepod
ersitina gasterostei (Pagenstecher, 1861) and
peritrich ciliate of the genus Trichodina were very
oen found attached to gills or gill covers, and dorsal
or pectoral ns, respectively. Nevertheless, parasite
diversity was relatively low compared to other studies
conducted in the Baltic Sea. In the checklist of
parasites of G. aculeatus, Morozińska-Gogol (2006)
mentioned 51 species (taxa) found on sticklebacks
in Poland. However, the number of parasite species
(21) is lower for sticklebacks from the Bothnian Gulf
(Valtonen et al. 2001) and two Norwegian lakes,
where a total of 14 macroparasite species or taxa
were recovered from sticklebacks, including eight
cestodes, one monogenean, one nematode and four
digeneans (Jakobsen 2011). Given the lack of detailed
data on macroscopic ectoparasites of sticklebacks
and their infection intensity from Puck Bay, more
data are needed to determine the impact of these
parasites on their sh host.
ere is a variety of ways that environmental
changes aect parasites, which indicate that
information on parasites can indicate anthropogenic
impact. In some instances, a parasite may be directly
susceptible to toxic eects of pollutants, in wh ich case
the pollution may reduce the infection prevalence
and intensity. If the host is more susceptible than
the parasite to a pollutant, its resistance to infection
may be reduced, leading to higher prevalence and
intensity. Parasitism may increase if the impact
reduces the host resistance or increases the density
of intermediate or denitive hosts. Parasitism may
be reduced if denitive or intermediate host density
declines or parasites suer higher mortality directly
(e.g. from toxic eects on parasites) or indirectly
(infected hosts suer by high mortality). Although
these scenarios are opposed to each other, they can
provide a rich set of predictions once we understand
the true associations between each parasite and the
eect (Laerty 1997). Many parasites have delicate
free-living transmission stages which are highly
sensitive to environmental change. A reduction in
their levels of infection will serve as an early warning
of changes. On the other hand, other parasites are
highly resistant to environmental change and will
respond by increased levels of infection. As a general
rule, infections with endoparasitic helminths tend
to decrease, while infections with ectoparasites
tend to increase with increasing levels of pollution
(Mackenzie 1999).
Morozińska-Gogol (2011) found a sharp increase
in the prevalence of S. solidus among sticklebacks
from the Gulf of Gdańsk in the period 1994-2008
and she argues that large-scale eutrophication
of the Baltic sea is responsible for this increase.
Eutrophication favors the existence of plants
and herbivores at the same time. Consequently,
herbivorous snails and crustaceans − the main
intermediate parasite hosts − usually dominate.
erefore, parasites can prot from eutrophication
(Reimer 1995). To some extent eutrophication also
increases the diversity of invertebrate species and has
an indirect positive eect on parasites with a complex
life cycle, like cestodes (Morozińska-Gogol 2011).
us, excessive eutrophication which is observed
every year in Puck Bay, and the growing population
of cormorants − the nal bird host both in the Gulf
of Gdańsk and Puck Bay − would result in much
higher prevalence and intensity of infection among
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16
Zdeněk Mačát, Adam Bednařík, Martin Rulík
www.oandhs.ocean.ug.edu.pl
Oceanological and Hydrobiological Studies, VOL. 44, ISSUE 1 | MA RCH 2015
©Faculty of Oceanography and Geography, University of Gdańsk, Poland. All rights reserved.
the studied sticklebacks. However, our average
prevalence values were lower compared to data
found by Morozińska-Gogol (2011) from the same
area. A likely explanation for the observed pattern is
that there might be a negative eect of pollution, like
eutrophication, leading to disruption of the parasite
S. solidus’ life cycle. Nevertheless, some additional
data regarding the density of copepods (rst parasite
hosts) or the assessment of the population size of
piscivorous birds (nal parasite hosts) are needed to
clarify the actual state of prevalence.
A
We would like to thank Krzysztof Skóra and the
sta of the Hel Marine Station of the University of
Gdańsk for their support in logistics. Radim Gabriš
and Stanislav Rada are acknowledged for their
valuable help in the eld and with statistics. Our stay
at the Hel Marine Station was funded by European
Social Fund CZ.1.07/2.2.00/28.0149.
References
Bańbura, J. (1994). Lateral plate morph dierentiation on
freshwater and marine populations of the three-spined
stickleback, Gasterosteus aculeatus, in Poland. Journal of Fish
Biology. 44: 773-783.
Barber, I. (2013). Sticklebacks as model hosts in ecological and
evolutionary parasitology. Trends in Parasitology. 29: 556-
566. DOI 10.1016/j.pt.2013.09.004.
Barber, I. & Huntingford, F.A. (1995). e eect of Schistocephalus
solidus (Cestoda: Pseudophyllidea) on the foraging
and shoaling behaviour of three-spinned sticklebacks,
Gasterosteus aculeatus. Behavio ur. 132: 1223-1240.
Barber, I. & Scharsack, J.P. (2010). e three-spined stickleback-
Schistocephalus solidus system: an experimental model for
investigating host-parasite interactions in sh. Parasitology.
137: 411-424. DOI 10.1017/S0031182009991466.
Bergersen, R. (1996). Sticklebacks from Greenland. Journal of
Fish Biology. 48: 799-801.
Bush, A.O., Laerty, K.D., Lotz, J.M. & Shostak, A.W. (1997).
Parasitology meets ecology on its own terms: Margolis et al.
revisited. Journal of Parasitology. 83: 575-583.
Carstensen, J., Andersen, J.H., Gustafsson, B.G. & Conley,
D.J. (2014a). Deoxygenation of the Baltic Sea during last
century. Proceedings of the National Academy of Sciences of
the United States of America. 111: 5628-5633. DOI 10.1073/
pnas.132315611.
Carstensen, J., Conley, D.J., Bonsdor, E., Gustafsson, B.G.,
Hietanen, S., Janas, U., Jilbert, T., Maximov, A., Norkko,
A., Norkko, J., Reed, D.C., Slomp, C.P., Timmermann, K. &
Voss, M. (2014b). Hypoxia in the Baltic Sea: Biogeochemical
cycles, benthic fauna, and management. AMBIO: A Journal
of the Human Environment. 43: 26–36. DOI 10.1007/s13280-
013-0474-7.
Chappell, L.H. (1969). e Parasites of the ree-spined
Stickleback Gasterosteus aculeatus L. from a Yorkshire
Pond. I. Seasonal Variation of Parasite Fauna. Journal of Fish
Biology. 1: 137-152.
Chubb, J.C., Ball, M.A. & Parker, G.A. (2009). Living in
intermediate hosts: evolutionary adaptations in larval
helminths. Trends in Parasitology. 26: 93-102. DOI 10.1016/j.
pt.2009.11.008.
Clarke, A.S. (1954). Studies on the life cycle of the
pseudophyllidean cestode Schistocephalus solidus.
Proceedings of the Zoological Society of London. 124: 257-302.
Confer, A., Vu, V., Drevecky, C.J. & Aguirre, W.E. (2012).
Occurrence of Schistocephalus solidus in anadromous
threespine stickleback. Journal of Parasitology. 98: 676-678.
DOI 10.1645/GE-2968.1.
Conley, D.J. (2012). Save the Baltic Sea. Nature. 486: 463-464.
DOI 10.1038/486463a.
Dingemanse, N.J., Oosterhof, Ch., Van der Plas, F. & Barber I.
(2009). Variation in stickleback head morphology associated
with parasite infection. Biological Journal of the Linnean
Society. 96: 759-768. DOI 10.1111/j.1095-8312.2008.01179.x.
Giles, N. (1983). Behavioural eects of the parasite Schistocephalus
solidus (Cestoda) on an intermediate host, the three-spined
stickleback, Gasterosteus aculeatus L. Animal Behaviour. 31:
1192-1194.
Hendry, A.P., Peichel, C.L., Matthews, B., Boughman, J.W. &
Nosil, P. (2013). Stickleback research: the now and the next.
Evolutionary Ecology Research. 15: 1-31.
Heins, D.C. & Baker, J.A. (2008). e stickleback-Schistocephalus
host-parasite system as a model for understanding the eect
of a macroparasite on host reproduction. Behaviour. 145:
625-645. DOI 10.1163/156853908792451412.
Hoberg, E.P., Henny, C.J., Hedstrom, O.R. & Grove, R.A. (1997).
Intestinal helminths of river otters (Lutra canadensis) from
the Pacic Northwest. Journal of Parasitology. 83: 105-110.
Hopkins, C.A. & Smyth, J.D. (1951). Notes on the morphology
and life history of Schistocephalus solidus (Cestoda,
Diphyllobothriidae). Parasitology. 41: 283-291.
Jäger, I. & Schjørring, S. (2006). Multiple infections: Relatedness
and time between infections aect the establishment
and growth of the cestode Schistocephalus solidus in its
stickleback host. Evolution. 60(3): 616-622. DOI: 10.1111/
j.0014-3820.2006.tb01141.x
Jakobsen, J. (2011). Parasite communities of two three-spined
stickleback (Gasterosteus aculeatus) populations - Eects
of a local-scale host introduction? MS thesis in Biology,
University of Trømso, 43 pp.
Kautsky, N., Kautsky, H., Kautsky, U. & Waern, M. (1986).
Decreased depth penetration of Fucus vesiculosus since the
Author's copy

17
The three-spined stickleback infection with Schistocephalus solidus
Oceanological and Hydrobiological Studies, VOL. 44, ISSUE 1 | MA RCH 2015
©Faculty of Oceanography and Geography, University of Gdańsk, Poland. All rights reserved.
1940’s indicates eutrophication of the Baltic Sea. Marine
Ecology Progress Series. 28: 1–8.
Laerty, K.D. (1997). Environmental parasitology: What can
parasites tell us about human impacts on the environment?
Parasitology Today. 13: 251-255.
Leppäkoski, E. & Olenin, S. (2000). Non-native species and rates
of spread: lessons from the brackish Baltic Sea. Biological
Invasions. 2: 151-163. DOI 10.1023/A:1010052809567.
Lobue, C.P. & Bell, M.A. (1993). Phenotypic manipulation by the
cestode parasite Schistocephalus solidus of its intermediate
host, Gasterosteus aculeatus, the threespine stickleback. e
American Naturalist. 142: 725-735.
Mackenzie, K. (1999). Parasites as pollution indicators in marine
ecosystems: a proposed Early Warning System. Marine
Pollution Bulletin. 38(11): 955-959. DOI 10.1016/S0025-
326X(99)00100-9.
MacColl, A.D.C. (2009). Parasite burdens dier between
sympatric three-spined stickleback species. Ecography. 32:
153-160. DOI 10.1111/j.1600-0587.2008.05486.x.
Marcogliese, D.J. (2005). Parasites of the superorganism: Are
they indicators of ecosystem health? International Journal for
Parasitology. 35: 705-716. DOI 10.1016/j.ijpara.2005.01.015.
Moore, J. (2002). Parasites and the behavior of animals. Oxford:
Oxford University Press.
Morozińska-Gogol, J. (2006). A checklist of parasites recorded
on stickleacks (Actinopterygii: Asterosteidae) from Poland.
Parasitology International. 55: 69-73. DOI 10.1016/j.
parint.2005.10.002.
Morozińska-Gogol, J. (2011). Changes in levels of infection
with Schistocephalus solidus (Müller, 1776) of the three-
spined stickleback Gasterosteus aculeatus (Actinopterygii:
Gasterosteidae) from the Gdynia Marina. Oceanologia. 53:
181-187. DOI 10.5697/oc.53-1.181.
NatureServe (2013). Gasterosteus aculeatus. e IUCN Red List
of reatened Species. Version 2014.2. Retrieved November
04, 2014, from www.iucnredlist.org
Ness, J.H. & Foster, S.A. (1999). Parasite-associated phenotype
modications in threespine stickleback. Oikos. 85: 127-134.
Ojaveer, H. & Kotta, J. (2006). Alien invasive species in the north-
easter Baltic Sea: populatiomn dynamics and ecological
impacts. Estonian Marine Institute Report No. 14: 64 pp.
Paavola, M., Olenin, S. & Leppäkoski, E. (2005). Are invasive
species most successful in habitats of low native species
richness across European brackish water seas? Estuarine,
Coastal and Shelf Science. 64: 738-750. DOI 10.1016/j.
ecss.2005.03.021.
Poulin, R., Blanar, C.A., ieltges, D.W. & Marcogliese, D.J.
(2011). e biogeography of parasitism in sticklebacks:
distance, habitat dierences and the similarity in parasite
occurrence and abundance. Ecography. 34: 540-551. DOI
10.1111/j.1600-0587.2010.06826.x.
Poulin, R. & omas, F. (1999). Phenotypic variability induced by
parasites: extent and evolutionary implications. Prasitology
Today. 15: 28-32.
Ranta, E. (1995). Schistocephalus infestation improves prey-
size selection by three-spined sticklebacks, Gasterosteus
aculeatus. Journal of Fish Biology. 46: 156-158.
Reimchen, T.E. & Nosil, P. (2001). Ecological causes of sex-biased
parasitism in threespine stickleback. Biological Journal of the
Linnean Society. 73: 51-63. DOI: 10.1111/j.1095-8312.2001.
tb01346.x
Reimer, L.W. (1995). Parasites especially of piscean hosts as
indicators of the eutrophication in the Baltic Sea. Applied
Parasitology. 36: 124-135.
Rolbiecki, L., Rokicki, J., Morozińska-Gogol, J. & Chibani,
M. (1999). Larval stages of helminths in sh from the
Vistula Lagoon and the Gulf of Gdańsk in relation to bird
occurrence. Bulletin of the Sea Fisheries Institute. 147: 51-60.
Rönnberg, C. & Bonsdor, E. (2004). Baltic Sea eutrophication:
area-specic ecological consequences. Hydrobiologia. 514:
227-241, DOI 10.1007/978-94-017-0920-0_21.
Rózsa, L., Reiczigel, J. & Majoros, G. (2000). Quantifying
parasites in samples of hosts. Journal of Parasitology. 86: 228-
232, DOI 10.1645/0022-3395(2000)086[0228:QPISOH]2.0.
CO;2.
StatSo, Inc. (2013). STATISTICA (data analysis soware
system), version 12. Retrieved November 04, 2014, from
www.statso.com.
Sures, B. (2004). Environmental parasitology: relevancy of
parasites in monitoring environmental pollution. Trends in
Parasitology. 20: 170-177. DOI 10.1016/j.pt.2004.01.014.
Tierney, J.F. (1994). Eects of Schistocephalus solidus (Cestoda)
on the food intake and diet of the three-spined stickleback,
Gasterosteus aculeatus. Journal of Fish Biology. 44: 731-735.
Valtonen, E.T., Pulkkinen, K., Poulin, R. & Julkunen, M.
(2001). e structure of parasite component communities
in brackish water shes of the northeastern Baltic Sea.
Parasitology. 122: 471-481.
Wootton, R.J. (1976). e biology of the sticklebacks. London:
Academic Press.
Zander, C.D. (1998). Ecology of host parasite relationships in the
Baltic Sea. Naturwissenschaen. 85: 426-36.
Zander, C.D. (2007). Parasite diversity of sticklebacks from the
Baltic Sea. Parasitology Research. 100: 287-297. DOI 10.1007/
s00436-006-0282-0.
Zander, C.D. & Kesting, V. (1996). e indicator properties of
parasites communities of gobies (Teleostei, Gobiidae) from
Kiel and Lübeck Bight. Applied Parasitology. 37: 186-204.
Zander, C.D. & Reimer, L.W. (2002). Parasitism at the ecosystem
level in the Baltic Sea. Parasitology. 124: 119-135. DOI
10.1017/S0031182002001567.
Zander, C.D., Strohbach, U. & Groenewold, S. (1993). e
importance of gobies (Gobiidae, Teleostei) as hosts and
transmitters of parasites in the SW Baltic. Helgoländer
Meeresuntersuchungen. 47: 81-111. DOI 10.1007/
BF02366186.
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