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Aquatic Invasions (2016) Volume 11, Issue 2: 189–198
DOI: http://dx.doi.org/10.3391/ai.2016.11.2.08
Open Access
© 2016 The Author(s). Journal compilation © 2016 REABIC
Research Article
Reduced survival of a native parasite in the invasive round goby:
evidence for the dilution hypothesis?
Andrée D. Gendron * and David J. Marcogliese
Aquatic Contaminants Research Division, Water Science and Technology Directorate, Environment and Climate Change Canada,
St. Lawrence Centre, 105 McGill, 7th Floor, Montreal, Quebec H2Y 2E7, Canada
*Corresponding author
E-mail: [email protected]
Received: 5 September 2015 / Accepted: 21 December 2015 / Published online: 15 February 2016
Handling editor: Vadim Panov
Abstract
With economic globalization, a growing number of exotic species are integrating into food webs outside their historical range, giving rise to the
development of novel associations between exotic hosts and local parasites. Depending on the parasite’s ability to survive and undergo
transmission, invasive exotic hosts can act as sinks or reservoirs for native parasites, thus either decreasing or increasing their overall abundance in
indigenous hosts. Here we evaluate the relative host competence of the invasive round goby ( Neogobius melanostomus) for a native
acanthocephalan species, Neoechinorhynchus tenellus, in the Great Lakes – St. Lawrence River basin. The second most abundant helminth
acquired by the round goby, N. tenellus was found to die prematurely in this novel paratenic (transport) host. On average, nearly half of the cysts
found in gobies sampled at 14 localities contained dead and degenerated cystacanths. Parasite remnants in hepatic tissues were surrounded by mast
cells indicative of an innate inflammatory host reaction. Conversely, cystacanths of N. tenellus were intact in johnny darters ( Etheostoma nigrum)
and logperch (Percina caprodes ), two co-occurring native paratenic hosts. We conclude that the round goby is currently a poor host for N. tenellus
relative to indigenous counterparts. As such, this abundant exotic fish could act as a sink and impair the transmission of N. tenellus, possibly
resulting in parasite dilution in native fish competitors. The significantly higher intensity and prevalence of infection in johnny darters at a goby-free
locality supports this hypothesis. However, this new host-parasite relationship might evolve with time toward an attenuation of the goby immune
defense reaction. Indeed, we found a negative correlation between the frequency of cystacanth degradation and time since gobies established in a
given locality, with the lowest degeneration rate in the St. Clair River area where the round goby was first recorded in the Great Lakes – St.
Lawrence basin. The dilution effect, if it exists, could then be temporary.
Key words: round goby, Neogobius melanostomus, acanthocephalan, host competence, dilution effect, Great Lakes, St. Lawrence River
Introduction
Host-parasite relationships are evolving ecological
interactions between antagonist partners. On their
part, hosts tend to evolve immune, physiological
and behavioral defenses to eliminate their parasites
or minimize their most deleterious effects
(Anderson and May 1982; Ebert and Hamilton 1996).
In response, parasites develop counter-strategies
to evade their host’s defense, using tactics such
as encapsulation, antigen mimicry or the
inhibition of specific immune functions (SitjàBobadilla 2008). Over the long term, coevolution
of hosts and parasites can sometimes result in
less hostile relationships whereby a cost-benefit
tradeoff is reached (Lenskit and May 1994; Alizon
et al. 2009). In such cases, pathogens may reduce
their virulence and/or hosts may increase their
tolerance for unavoidable parasites.
In a globalized world, species invading new
habitats outside their native range are likely to
shake these long-lasting relationships and provide
opportunities for the development of novel hostparasite associations (Lafferty et al. 2005; Nelson et
al. 2015b). Indeed, introduced species carry some
of their parasites into the invaded habitats,
bringing them into contact with a large pool of
potential new hosts (Lymbery et al. 2014). Most
of these exotic parasites do not find the suitable
hosts that would ensure their survival (Dobson
and May 1986); a few, however, not only survive
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A.D. Gendron and D.J. Marcogliese
but become invasive, sometimes causing significant
damage to their new hosts (Taraschewski 2006;
Choudhury and Cole 2011; Lymbery et al. 2014).
Once established, exotic species can find themselves
exposed to local parasites. Although parasite
communities in exotic species tend to remain
less diverse than conspecific host populations in
native habitats (Torchin and Mitchell 2004) and
than local competitors in the invaded habitats
(Gendron et al. 2012), native parasite acquisition
does occur over time and has been reported in a
number of recent studies (Telfer et al. 2005;
Gendron et al. 2012; Paterson et al. 2012; Sheath
et al. 2015).
Until now, efforts to understand the influence
of exotic species on native host-parasite dynamics
have identified two main divergent outcomes. If
an introduced species becomes a competent host
to a given native parasite – allowing it to survive
and be transmitted further – it may act as a
reservoir of infection and eventually lead to an
overall increase in the abundance of this parasite
among indigenous hosts, termed parasite spillback
(Kelly et al. 2009a; Poulin et al. 2011). Alternatively,
if a native parasite is acquired by an unsuitable
introduced host which acts as a sink (or dead-end)
for that parasite, a dilution effect may ensue,
whereby indigenous hosts experience a decrease
in infection by that parasite (Telfer et al. 2005;
Kopp and Jokela 2007; Paterson et al. 2011;
Lettoof et al. 2013).
The main objective of this study was to assess
the competence of an invasive fish, the round
goby (Neogobius melanostomus Pallas, 1814), to
host a native parasite, Neoechinorhynchus tenellus
(Van Cleave, 1913). The round goby is an introduced
Eurasian fish now widespread and abundant in
the Great Lakes – St. Lawrence River basin
(Brodeur et al. 2011; Kornis et al. 2012) where it
is parasitized by a small number of local parasite
species (none being exotic), most frequently by
the generalist digenetic trematode Diplostomum
spp. (Muzzal et al. 1995; Kvach and Stepien 2008;
Gendron et al. 2012). Of the twenty-some native
helminths acquired so far by gobies in the St.
Lawrence River, the acanthocephalan N. tenellus
is the second most prevalent and abundant
(Gendron et al. 2012). This species is transmitted
to fish by the ingestion of infected ostracods
(Walkey 1967; Uglem and Larson 1969), an important
component of the diet of juvenile round gobies
(Gendron et al. 2012). They mature in the digestive
tract of their definitive host, usually a piscivorous
fish (Amin and Muzzall 2009), releasing embryonated
eggs that are passed in the feces and subsequently
190
eaten by ostracods (Walkey 1967; Uglem and Larson
1969; Kennedy 2006). In round gobies however,
and in some indigenous benthic percids, N. tenellus
rarely establishes in the digestive tract; rather it
penetrates the gut and encysts in the viscera as a
cystacanth. These fish are utilized as paratenic or
transport hosts and are optional components of
the parasite’s life cycle; they must be consumed
by a suitable definitive fish host for cysacanths
to develop into adults and reproduce (Kennedy
2006). Considering that the round goby has become
a dominant species in the Great Lakes and the St.
Lawrence River (Kipp et al. 2012) and is now an
important part of the diet of a number of
piscivorous fish (Reyjol et al. 2010), it has the
potential to influence the population dynamics
and transmission of N. tenellus among native fish
(causing dilution or spillback), depending on its
competence as a host relative to native hosts. To
further explore this hypothesis, we compared the
prevalence and intensity of infection as well as
the survival of N. tenellus in the exotic round
goby in the St. Lawrence River and lower Great
Lakes with that of two native paratenic hosts, the
johnny darter (Etheostoma nigrum Rafinesque, 1820)
and the logperch (Percina caprodes Rafinesque,
1818), which presumably have a long-standing
association with N. tenellus.
Material and methods
Study area and fish sampling
Fish were sampled in the Great Lakes – St. Lawrence
basin during the summer months, between 2006
and 2014, using a beach seine (22.6 m × 1.15 m;
3 mm mesh) pulled by hand or partially deployed
from a boat. Samples of round gobies were obtained
from 17 sites ranging from Lake St. Clair to Lake
St. Pierre (Figure 1, supplementary material Table
S1). At 8 of these localities, samples of johnny
darter (Etheostoma nigrum) or logperch (Percina
caprodes), two native benthic percid fish, were
collected as well. In addition, a sample of johnny
darter was obtained from a reference area not yet
colonized by the round goby. Upon capture, fish
were euthanized in a 400 mg/L Eugenol (clove oil)
solution (American Veterinary Medical Association
2013), individually bagged and frozen for subsequent
parasitological examination. A small number of
fish were brought live to our laboratory where they
were maintained in indoor tanks for a short period
of time until being processed. These were used
as a source of voucher parasite specimens and
for histological examination of infected tissues.
Interaction between an invasive fish and a native parasite
Figure 1. Sampling locations in the Great Lakes (A) and the St. Lawrence River (B). Fill color of circles designates which fish species were
collected at a given locality: Black stands for the round goby (Neogobius melanostomus), gray for the johnny darter (Etheostoma nigrum) and
white for the logperch (Percina caprodes). SCA= Lake St Clair-Anchor Bay, PUB=Puce Beach, KIN=Kingsville, HAH=Hamilton Harbour,
COR=Cornwall, BEA=Beauharnois, IPA=Îles de la Paix, ILO=Île de la Couvée, CME=Cap-sur-mer, Q56=Quay 56, PBE=Promenade Bellerive,
IGR=Île Gros Bois, IVT=Îlet Vert, IDC=Îles de Contrecoeur, LAV=Lavaltrie, SOR=Sorel, IAO=Île aux Ours, PDL=Pointe du lac. For details see
supplementary material Table S1.
Parasitological examination
Prior to dissection, standard length was measured
to the nearest mm and each fish was weighed to
the nearest 0.01 g. The abdominal organs were
removed and examined using a stereomicroscope.
Squash preparations of liver, kidney, mesenteries
and intestinal wall were made to reveal encysted
acanthocephalans (cystacanths). The content of
the gastro-intestinal tract also was searched for
adult worms. Acanthocephalans found were excysted
and classified as intact or partially degenerated
and counted. Cleaned specimens were fixed in
70% ethanol before being stained in acetocarmine,
cleared in clove oil, and mounted on slides.
Specimens were identified to species on the basis
of morphological criteria following keys in Arai
(1989) and taking into account recent redescriptions and revisions within the genus
Neoechinorhynchus (Amin 2002; Amin and Muzzall
2009). Morphological measurements were made
using the software Leica IM1000 (V4.0) connected
to a DC500 digital camera mounted on a Leica
DMR microscope. Voucher specimens of N. tenellus
(ROMIZ F320; ROMIZ F320) have been deposited
in the Royal Ontario Museum (Toronto, Canada).
Histology of parasitized tissues
Round gobies collected in 2009 at Île de la Couvée
(ILO), a locality of elevated prevalence of infection
by cystacanths, were transported alive to the laboratory and processed for histological examination.
Livers of infected fish were rapidly removed and
small blocks containing visible cysts were fixed
in 10% neutral buffered formalin prior to being
sent to a professional histology laboratory (The
Centre for Bone and Periodontal Research, McGill
University, Montreal, Canada). There, tissues were
dehydrated with a graded series of ethanol, embedded
in paraffin and sectioned at 4 µm. Liver sections
from 15 gobies underwent hematoxylin-eosin
(H&E), periodic acid Schiff (PAS), Perls' Prussian
blue or Toluidine blue staining and were evaluated
qualitatively using the image analysing system
previously described. Aspects considered include
parasite integrity, cyst structure and signs of
immune reaction (degranulation).
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A.D. Gendron and D.J. Marcogliese
Parasite parameters and statistical analyses
Parasitological descriptors are defined in Bush et
al. (1997). Prevalence is the percentage of
infected fish in a given sample, mean intensity is
the mean number of parasites per infected host in
a sample whereas mean abundance is the mean
number of parasites per host be it infected or not.
Fulton’s condition factor (K) was calculated as
W/L3 where W is the weight of the fish in gm
and L is the standard length in mm (Ricker
1975). Data were analysed using SAS release 9.4
(SAS Institute Inc., Cary, NC, USA). The mean
abundance of N. tenellus was compared among
localities and between host species through oneway analyses of variances (ANOVA) performed
on rank-transformed data using a normal score
transformation instead of standard ranks (Conover
1999). When more than two samples were compared,
the ANOVA was followed by Tukey-Kramer
multiple comparisons of means. Correlation analyses
were performed to measure the association between
parasite intensity and host-related variables (size,
length, condition). When the assumption of linearity
could be met (using raw or an arithmetic transformation of data), Pearson’s coefficient was
calculated. Otherwise, the association was measured
using Spearman’s rank correlation coefficient.
The relationship between infection parameters
and time since establishment of the round goby
was examined using localities where the documented
year of detection was established.
Results
Round gobies were infected by N. tenellus at 12
out of 14 localities sampled in the St. Lawrence
River and at 2 out of 4 localities in the Great
Lakes (Table S2, Figure 2). Overall, the parasite
was present in 27% of the gobies examined at a
mean intensity of 3.2. However, infection levels
varied considerably from one locality to another
(Figure 2), reaching highs at Beauharnois (BEA;
prevalence: 85%; mean intensity: 3.7) and Île de
la Couvée (ILO; prevalence: 93%; mean intensity:
6.6) where as many as 36 acanthocephalans were
found in a single fish host. The native johnny
darter was also a frequent host for N. tenellus
(Table S2, Figure 3). The prevalence and intensity
of infection in darters fluctuated among sites
around an overall mean prevalence of 30% and a
mean intensity of 2.7. At Île aux Ours (IAO), a
site where the round goby has not yet established,
the mean abundance of acanthocephalans in the
192
Figure 2. Infection of round gobies (Neogobius melanostomus) by
Neoechinorhynchus tenellus in the Great Lakes - St. Lawrence basin.
Locations shown are those where at least one goby was infected by
the parasite. A. Bars reflect the intensity of infection expressed as the
mean number of acanthocephalans – intact and degraded – per
infected fish ± SEM. B. Prevalence is the percent fish parasitized by
N. tenellus.
johnny darter was significantly higher (P<0.0001)
than at all other localities. Each fish examined
from IAO was parasitized by N. tenellus with a
mean intensity of 4.33 (Table S2). In comparison,
N. tenellus was less prevalent and abundant in
the tissues of logperch (Table S2, Figure 3).
Only 3% of all logperch examined in this study
were parasitized by this acanthocephalan species. As
in the round goby, the prevalence and mean intensity
were more elevated at Île de la Couvée (ILO), with
values of 18% and 1.6 respectively.
Only one adult N. tenellus was found in the
intestine of the round goby. In both the invasive
host and the native fish hosts studied, the
acanthocephalans remained at an immature stage
(cystacanth). They were found encapsulated in
the body cavity in association with the intestinal
wall or mesenteries or, more frequently, within
the liver (Figure 4). Except for one specimen, all
acanthocephalans excysted from the logperch
and the johnny darters showed no signs of
degradation. In contrast, cystacanths regularly
were found partly degenerated in the round goby
(Figure 4). Cysts of degraded acanthocephalans
were surrounded by mast cells and free granules
(degranulation) were visible in the infected region
(Figure 5). In several instances, the proboscis
hard parts were the only remaining identifiable
structures in the cysts (Figure 5d).
Interaction between an invasive fish and a native parasite
Figure 3. Comparison in the level of infection by Neoechinorhynchus
tenellus between the round goby (Neogobius melanostomus) and the
two native fish hosts, the johnny darter (Etheostoma nigrum) and
the logperch (Percina caprodes). A. Prevalence: each bar displays
the percentage of fish parasitized by N. tenellus. B. Intensity of
infection is expressed as the average number of N. tenellus among
infected fish. Error bars shown are SEM. The round goby was found
at all locations but one (IAO).
The frequency of degraded acanthocephalans
in round gobies fluctuated between 0% and 66%
(47% on average) depending on locality (Figure
2) and was negatively correlated (P=0.005;
r=-0.84) with the estimated time since gobies
became established in a given locality (Figure 6).
Indeed, the lowest levels of parasite degradation
occurred at two localities in the St. Clair River
area, where the round goby was first reported in
the Great Lakes at the beginning of the 1990s.
Morphometric measurements of the three fish
hosts are presented in Table S2. We found no
significant relationship between the level of infection
by N. tenellus and the size, weight or condition in
the round goby and the two native species except
at Île aux Ours (IAO) where the condition index
of johnny darters significantly decreased with
the intensity of infection (rho=-0.57, P=0.0068).
Figure 4. Death and degeneration of cystacanths in tissues of the
exotic round goby (Neogobius melanostomus) (A) in comparison to
the native johnny darter (Etheostoma nigrum) (B) and logperch
(Percina caprodes) (C). Stacked bars cumulate the mean number of
whole (intact) and degraded cystacanths for each fish host (all
locations pooled). Error bars refers to SEM.
Discussion
Neoechinorhynchus tenellus is one of the few
native parasites acquired by the exotic round
goby since its introduction in the Great Lakes –
St. Lawrence River basin in the 1990s (Gendron
et al. 2012). Prevalence of infection by this parasite
can reach as much as 93% locally and mean
intensity as many as 7 worms per fish. However,
results presented herein indicate that N. tenellus
experiences high mortality in its novel host.
Indeed, we found that, on average, half of the
acanthocephalans encysted in the internal organs
of gobies from the St. Lawrence River, were
dead and degraded.
193
A.D. Gendron and D.J. Marcogliese
Figure 5. Photomicrographs of
Neoechinorhynchus tenellus encysted in
the liver of the round goby (Neogobius
melanostomus). A. Acanthocephalan
cyst (asterisk) protruding from fish
hepatic tissues; bar=3 mm. B.
Acetocarmine stained, in toto preparation
of a typical adult; H=rows of hooks;
P=proboscis; PR=proboscis receptacle;
L=lemnisci; T=testis; M=macronuclei;
bar=200 µm. C. Anterior region of an
intact cystancanth. Note the proboscis (P)
and the large apical hooks (AH)
characteristic of the species; PR =
Proboscis receptacle; bar=50 µm. D. A
degraded cystacanth showing remains of
body tissue (asterisk). The proboscis (P)
hard parts, including the apical hooks
(AH) are the only remaining identifiable
structures bar=50 µm. E. Section of an
infected liver (H&E stained) showing
host tissue structure around an intact
cystacanth; P= proboscis;
Asterisk=anterior body; bar=50 µm. F.
Section of hepatic tissues with numerous
mast cells (M) surrounding the cyst of a
partly degraded acanthocephalan. Note
the degranulation of mast cells
(arrowhead) visible nearby the proboscis
(P); large apical hooks=AH; cyst
wall=CW; bar=50 µm.
Figure 6. Correlation between percent cystacanth degradation in
tissues of the round goby (Neogobius melanostomus) and time since
its establishment in a given locality. SCA= Lake St Clair-Anchor
Bay, PUB=Puce Beach, COR=Cornwall, BEA=Beauharnois,
IPA=Îles de la Paix, ILO=Île de la Couvée, CME=Cap-sur-mer,
Q56=Quay 56, IGR=Île Gros Bois.
194
In the Black Sea, the Sea of Azov and the other
parts of its Eurasian range, the round goby is
commonly parasitized by several marine, brackish
and/or freshwater acanthocephalans, including
species of the genus Acanthocephalus, Acanthocephaloides, Pomphorhynchus, Telosenti (Kvach
(2002, 2005, 2006) and occasionally Neoechinorhynchus (N. rutili Miller, 1880) (Özer 2007).
These helminths, which often dominate the parasite
communities of gobies locally, either encyst in
the viscera and remain as cystacanths and/or
develop into gravid adults in the intestine then
using gobies as definitive hosts (e.g. N. rutili; A.
propinquus Dujardin, 1845). To our knowledge,
there is no published mention of degradation or
any other signs of premature death of cystacanths
infecting gobies in their native habitats or other
parts of their extended distribution in Europe
(Kvach and Winkler 2011; Emde et al. 2012).
Parasite death in host tissue may go unnoticed,
overlooked or be considered irrelevant to reporting
Interaction between an invasive fish and a native parasite
unless it is the focus of research. In this study,
cystacanth degradation was clearly a phenomenon
unique to gobies whereas virtually all acanthocephalans recovered from two native paratenic
fish hosts – the johnny darter and the logperch –
were intact. Moreover, histological assessment
revealed mobilization of mast cells and their
degranulation around cystacanth remnants in gobies,
suggestive of a vigorous host reaction to infection.
Mast cells are inflammatory cell types involved in
the innate immune response of fish to parasitic
helminths, including acanthocephalans (Dezfuli et al.
2008).
Similar results were reported by Kelehear and
Jones (2010) who studied the establishment of
native larval nematodes (Spirurida) in the invasive
cane toad (Rhinella marina=Bufo marinus Linnaeus,
1758) in Australia. These authors found evidence
of a marked immune response in the host tissues,
including cellular infiltration and fibrotic reaction
around the parasites leading to calcification and
parasite destruction. In contrast, nematode infection
rarely provoked such exacerbated reaction in
native frog hosts, presumably reflecting the long
evolutionary association between them. In
another study where metamorphs of cane toads
were experimentally exposed to native lungworms
(Rhabdias spp.), infective larvae were able to
penetrate the skin and migrate through the body
of the exotic toads but none reached the target
tissue – the lungs – where they mature and reproduce
(Nelson et al. 2015b). Most immature nematodes
establishing in non-target tissues did not survive
and many were found disintegrating and invaded
by immune cells.
Using a combination of field survey and experimental infection, Paterson et al. (2013) also
observed low establishment and survival of two
generalist native trematodes in exotic salmonids,
Salmo trutta (Linnaeus, 1758) and Oncorhynchus
mykiss (Walbaum, 1792), in New Zealand. The
authors concluded that the introduced fish were
poor hosts for both native helminths and that
they could contribute to reducing trematode
transmission to the main native hosts over the
long term. Our results also suggest that the exotic
round goby is a poorly competent paratenic host
for N. tenellus in the St. Lawrence River, relative
to indigenous fish hosts fulfilling the same
ecological function for the parasite. With the
increasing density of round gobies in the St.
Lawrence River (up to 6 gobies/m2: Kipp et al.
(2012)) and their juveniles feeding heavily on
ostracods (Gendron et al. 2012) – the intermediate
hosts of N. tenellus – we suspect that this exotic
fish could act as a sink or dead-end for a large
number of these acanthocephalans. Assuming that
a significant part of the available larval pool of
N. tenellus ends up in the goby, premature death of
cystacanths before gobies are consumed by suitable
definitive hosts should result in a net loss of infective
stages from the system, ultimately causing a decrease
in the overall parasite population size.
This phenomenon, termed dilution effect, has
been described in a number of host-parasite systems
after changes in species composition and/or richness
following events such as bioinvasion (Keesing et
al. 2006; Johnson et al. 2008; Kelly et al. 2009b;
Johnson and Thieltges 2010; Lettoof et al. 2013).
For instance, cane toad invasion in Australia was
associated with a general reduction in parasite
burden in co-occurring native frogs (Lettoof et
al. 2013). In New Zealand streams, Kelly et al.
(2009b) found that the introduced brown trout
diluted infection by helminths in native fish in
direct relation to its abundance. Density-dependent
dilution effects were reported in a few other
epidemiological studies that were also replicated
experimentally (Nelson et al. 2015a). Experiments
with mussels raised in laboratory mesocosms
revealed that non-indigenous hosts acted as decoys
for the infective stages of native parasites, thus
reducing the risk of indigenous hosts becoming
infected, with greater reductions of infection levels
at higher invader densities (Thieltges et al. 2008).
The round goby now occurs in a variety of
habitats throughout the St. Lawrence River and
the Great Lakes. Localities not yet colonized by
the species are few, which complicated the
comparison of N. tenellus infection in indigenous
hosts between habitats with and without gobies.
Only one of our sampling sites turned out to be
goby-free. Interestingly, the prevalence and mean
intensity of N. tenellus in johnny darter at that
locality was more than double those at all other
sites where darters co-occurred with gobies. This
observation suggests that the introduction of an
invasive incompetent host has resulted in native
paratenic hosts becoming less parasitized. However,
more extensive surveys of the abundance of N.
tenellus in indigenous fish including yet-to-be
invaded areas in tributaries of the St. Lawrence
River, should be conducted before concluding
that the round goby has induced a dilution effect.
Further research should also assess the infection
levels in the obligatory hosts of N. tenellus including
its definitive hosts. Given that definitive hosts of
N. tenellus are piscivorous fish such as the northern
pike and the walleye (Amin and Muzzall 2009),
a significant portion of their infections probably
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A.D. Gendron and D.J. Marcogliese
is acquired through the consumption of infected
fish and less through direct ingestion of the
invertebrate intermediate hosts (ostracods), making
paratenic hosts key components in the life cycle
of this parasite. For a reduction in N. tenellus
infection to occur in definitive hosts, the increase
in the abundance of gobies should be paralleled
with a decrease in the abundance of native
paratenic hosts. In the Great Lakes, darters and
other benthic fish were found to decline significantly
following gobies invasion presumably due to
competition for food and space (Lauer et al.
2004) and the same appears to be occurring now
in the St. Lawrence River. In our seines, gobies
typically outnumbered johnny darters and logperch
(following a ratio of 10 to 1) in areas where
these two indigenous percids used to be abundant
(data not shown). Therefore, it appears that competent
indigenous hosts (johnny darters), which play an
important role in the transmission of N. tenellus
to its definitive host, are being replaced with a
poor exotic host (round gobies). The net influence of
gobies on the infection dynamics of definitive
hosts (dilution or amplification) will very much
depends on the relative rates of predation of
gobies vs other paratenic hosts along with the
specific survival rates of cystacanths in gobies,
which is difficult to predict from existing
information and will need to be addressed in
further studies.
Parasite dilution may represent one of the few
benefits conveyed by exotic species to invaded
communities (Kopp and Jokela 2007; Kelly et al.
2009b). Here, a reduction in the intensity of
infection by N. tenellus driven by the round goby
could hypothetically improve the health of native
fish competitors. Generally speaking, acanthocephalans are not responsible for major vertebrate
host die-offs, although they can on occasion
reach densities at which they cause epizootics
(Kennedy 2006). Nonetheless, they regularly induce
local damage to their fish hosts manifested as
inflammation and accumulation of fibrous tissues
at the site of infection, as well as gut perforation
and damage to internal organs as the parasite
migrates toward the sites of encystment in
paratenic hosts (Dezfuli et al. 2008). Intestinal
occlusions may also occur in highly infected
definitive hosts and result in significant weight
loss. A few studies have linked infection by
acanthocephalan to a reduction in host body
condition (Kennedy 2006; Thilakaratne et al. 2007),
an effect seen here in johnny darters at the gobyfree locality. At that site, N. tenellus dominated
the parasite fauna of johnny darters, accounting
196
for 50% of the total number of helminths infecting
their tissues, whereas the acanthocephalan represented
less than 10% of johnny darters’ parasite load at
sites where they coexisted with round gobies
(A.D. Gendron and D. Marcogliese, unpublished data).
This novel host-parasite relationship likely
will evolve over the years, most probably toward
a reduction in the defense mounted by the exotic
host against the native parasite. Our results
suggest that this is already occurring in the Great
Lakes, where the degradation rate of cystacanths
in gobies is significantly reduced compared to
what is observed in more recently established
populations in the St. Lawrence River. Although
this needs to be confirmed by more extensive
surveys, a rapid co-adaptation would not be
surprising considering the circumpolar distribution
of Neoechinorhynchus and the fact that other
species of this genus were found to infect the
round goby in its European native range (Özer
2007). As it progressively develops into a more
competent paratenic host, the influence of the
round goby in the transmission of N. tenellus in
the Great Lakes – St. Lawrence basin might
eventually switch from a putative dilution effect
to a spillback effect. Round gobies could then
facilitate the dissemination of that native parasite
and increase the intensity and prevalence of
infection in its main predators – saugers, walleyes
and northern pikes (Reyjol et al. 2010) – which
are known definitive hosts of N. tenellus (Amin
and Muzzall 2009).
Acknowledgements
We would like to thank Germain Brault, Michel Arsenault, Claude
Lessard, Sophie Trépanier, John Forest, Maude Lachapelle, Rebecca
Gouge, Xavier Bordeleau, Marie-Pier Ricard, Jacinthe Gosselin,
Eugénie Schaff, Pierre-Olivier Benoit, Maxime Guerard, JeanFrançois Lafond, Hubert Désilets, Lila Gagnon-Brambilla, Roxane
Petel and Maxime Thibault for their help in the collection of gobies
from the St. Lawrence River and/or examination of fish for parasites.
Round gobies from the Great Lakes were collected by Michael
Thomas of the Lake St. Clair Fisheries Research Station (Michigan,
USA), Lynda D. Corkum of the University of Windsor (Ontario,
Canada) and Marten Koops of the Department of Fisheries and
Oceans (Ontario, Canada). The histological services were provided
by the Centre for Bone and Periodontal Research of McGill
University (Quebec, Canada). This study was carried out as part of
the St. Lawrence Action Plan.
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The following supplementary material is available for this article:
Table S1. Sampling locations and records of studied species in the Great Lakes and the St. Lawrence River between 2006 and 2014.
Table S2. Morphometric data of round gobies (Neogobius melanostomus), logperch (Percina caprodes) and johnny darter
(Etheostoma nigrum) and mean abundance of Neoechinorhynchus tenellus at 18 locations in the Great Lakes – St. Lawrence basin.
This material is available as part of online article from:
http://www.aquaticinvasions.net/2016/Supplements/AI_2016_Gendron_Marcogliese_Supplement.xls
198