Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
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 189 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). 191 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 195 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. References Alizon S, Hurford A, Mideo N, Van Baalen M (2009) Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. Journal of Evolutionary Biology 22: 245– 259, http://dx.doi.org/10.1111/j.1420-9101.2008.01658.x Interaction between an invasive fish and a native parasite American Veterinary Medical Association (2013) The AVMA Guidelines for the Euthanasia of Animals. Schaumburg, IL, pp 102 Amin OM (2002) Revision of Neoechinorhynchus Stiles and Hassall, 1905 (Acanthocephala: Neoechinorhychidae) with keys to 88 species in two subgenera. Systematic Parasitology 53: 1–18, http://dx.doi.org/10.1023/A:1019953421835 Amin OM, Muzzall PM (2009) Redescription of Neoechinorhynchus tenellus (Acanthocephala: Neoechinorhynchidae) from Esox lucius (Esocidae) and Sander vitreus (Percidae), among other percid and centrarchid fish, in Michigan, U.S.A. Comparative Parasitology 76: 44–50, http://dx.doi.org/10.1654/4373.1 Anderson R, May R (1982) Coevolution of hosts and parasites. Parasitology 85: 411–426, http://dx.doi.org/10.1017/S00311820000 55360 Arai HP (1989) Acanthocephala. In: Margolis L, Kabata Z (eds), Guide to the parasites of fishes of Canada Part III. Canadian Special Publication of Fisheries and Aquatic Sciences Vol 107, pp 1–90 Brodeur P, Reyjol Y, Mingelbier M, Rivière T, Dumont P (2011) Prédation du gobie à taches noires par les poissons du SaintLaurent : contrôle potentiel d’une espèce exotique ? La Société Provancher d'Histoire Naturelle du Canada 135: 4–12 Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J. of Parasitology 83: 575–583, http://dx.doi.org/10.2307/3284227 Choudhury A, Cole R (2011) Bothriocephalus acheilognathi Yamaguti (Asian tapeworm). In: Francis RA (ed), A Handbook of Global Freshwater Invasive Species. Earthscan, London, U.K, pp 389–404 Conover W (1999) Practical non-parametric statistics. John Wiley and Sons, New York, pp 584 Dezfuli B, Giovinazzo G, Lui A, Giari L (2008) Inflammatory response to Dentitruncus truttae (Acanthocephala) in the intestine of brown trout. Fish and Shellfish Immunology 24: 726–733, http://dx.doi.org/10.1016/j.fsi.2007.11.013 Dobson A, May R (1986) Patterns of invasions by pathogens and parasites. In: Mooney HA, Drake JA (eds), Ecology and Biological Invasions of North America and Hawaii. Springer-Verlag, Berlin, pp 58–76, http://dx.doi.org/10.1007/978-1-4612-4988-7_4 Ebert D, Hamilton W (1996) Sex against virulence: The coevolution of parasitic diseases. Trends in Ecology and Evolution 11: 79– 82, http://dx.doi.org/10.1016/0169-5347(96)81047-0 Emde S, Rueckert S, Palm H, Klimpel S (2012) Invasive PontoCaspian amphipods and fish increase the distribution range of the acanthocephalan Pomphorhynchus tereticollis in the River Rhine. PLoS ONE 7: e53218, http://dx.doi.org/10.1371/journal. pone.0053218 Gendron A, Marcogliese D, Thomas M (2012) Invasive species are less parasitized than native competitors, but for how long? The case of the round goby in the Great Lakes-St. Lawrence Basin. Biological Invasions 14: 367–384, http://dx.doi.org/10.1007/s105 30-011-0083-y Johnson P, Hartson R, Larson D, Sutherland D (2008) Diversity and disease: community structure drives parasite transmission and host fitness. Ecology Letters 11: 1017–1026, http://dx.doi.org/10. 1111/j.1461-0248.2008.01212.x Johnson PTJ, Thieltges DW (2010) Diversity, decoys and the dilution effect: how ecological communities affect disease risk. Journal of Experimental Biology 213: 961–970, http://dx.doi.org/ 10.1242/jeb.037721 Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecology Letters 9: 485–498, http://dx.doi.org/ 10.1111/j.1461-0248.2006.00885.x Kelehear C, Jones HI (2010) Nematode larvae (Order Spirurida) in gastric tissues of Australian anurans: a comparison between introduced can toad and sympatric native frogs. Journal of Wildlife Diseases 46: 1126–1140, http://dx.doi.org/10.7589/00903558-46.4.1126 Kelly DW, Paterson RA, Towensend CR, Poulin R, Tompkins DM (2009a) Parasite spillback: A neglected concept in invasion ecology? Ecology 90: 2047–2056, http://dx.doi.org/10.1890/08-1085.1 Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009b) Has the introduction of brown trout altered disease patterns in native New Zealand fish? Freshwater Biology 54: 1805–1818, http://dx.doi.org/10.1111/j.1365-2427.2009.02228.x Kennedy CR (2006) Ecology of the Acanthocephala. Cambridge University Press, New York, pp 249, http://dx.doi.org/10.1017/ cbo9780511541902 Kipp R, Hébert I, Lacharité M, Ricciardi A (2012) Impacts of predation by the Eurasian round goby (Neogobius melanostomus) on molluscs in the upper St. Lawrence River. Journal of Great Lakes Research 38: 78–89, http://dx.doi.org/10. 1016/j.jglr.2011.11.012 Kopp K, Jokela J (2007) Resistant invaders can convey benefits to native species. Oikos 116: 295–301, http://dx.doi.org/10.1111/ j.0030-1299.2007.15290.x Kornis MS, Mercado-Silva N, Vander Zanden MJ (2012) Twenty years of invasion: a review of round goby Neogobius melanostomus biology, spread and ecological implications. Journal of Fish Biology 80: 235–285, http://dx.doi.org/10.1111/ j.1095-8649.2011.03157.x Kvach Y (2002) Helminths of goby fish of the Hryhoryivsky Estuary (Black Sean, Ukraine). Vestnik zoologii 36: 71–76 Kvach Y (2005) A comparative analysis of helminth faunas and infection parameters of ten species of gobiid fishes (Actinopterygii: Gobiidae) from the North-Western Black Sea. Acta Ichthyologica et Piscatoria 35: 103–110 Kvach Y (2006) A morphological study of Acanthocephaloides propinquus (Acanthocephala, Aryhthmacanthidae) parasitising gobiid fishes (Teleostei, Gobiidae) in the northwestern Black Sea. Acta Parasitologica 51: 59–64, http://dx.doi.org/10.2478/ s11686-006-0008-6 Kvach Y, Stepien C (2008) Metazoan parasites of introduced round and tubenose gobies in the Great Lakes: Support for the “enemy release hypothesis”. Journal of Great Lakes Research 34:23–35, http://dx.doi.org/10.3394/0380-1330(2008)34[23:MPOIRA]2.0.CO;2 Kvach Y, Winkler HM (2011) The colonization of the invasive round goby Neogobius melanostomus by parasites in new localities in the southwestern Baltic Sea. Parasitological Research 109: 769–780, http://dx.doi.org/10.1007/s00436-011-2321-8 Lafferty KD, Smith KF, Torchin ME, Dobson AP, Kuris AM (2005) The role of infectious diseases in natural communities: What introduced species tell us. In: Sax DF, Stachowicz JJ, Gaines SD (eds), Species Invasions: Insights into Ecology, Evolution and Biogeography. Sinauer Associates, Sunderland, pp 111–134 Lauer T, Allen P, McComish T (2004) Changes in mottled sculpin and johnny darter trawl catches after the appearance of round gobies in the Indiana waters of Lake Michigan. Transactions of the American Fisheries Society 133: 185–189, http://dx.doi.org/ 10.1577/T02-123 Lenskit R, May R (1994) The evolution of virulence in parasites and pathogens: reconciliation between two competing hypothesis. Journal of Theoretical Biology 169: 253–265, http://dx.doi.org/ 10.1006/jtbi.1994.1146 Lettoof DC, Greenlees MJ, Stockwell M, Shine R (2013) Do invasive cane toads affect the parasite burdens of native Australian frogs? International Journal for Parasitology: Parasites and Wildlife 2: 155–164, http://dx.doi.org/10.1016/j.ijp paw.2013.04.002 Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL (2014) Co-invaders: The effects of alien parasites on native hosts. International Journal for Parasitology: Parasites and Wildlife 3: 171–177, http://dx.doi.org/10.1016/j.ijppaw.2014.04.002 Muzzal P, Peebles C, Thomas M (1995) Parasites of the round goby, Neogobius melanostomus, and tubenose goby, Proterorhinus marmoratus (Perciformes: Gobiidae), from the St. Clair River and Lake St. Clair, Michigan. Journal of the Helminthological Society of Washington 62: 226–228 197 A.D. Gendron and D.J. Marcogliese Nelson FBL, Brown GP, Shilton C, Shine R (2015a) Helpful invaders: Can cane toads reduce the parasite burdens of native frogs? International Journal for Parasitology: Parasites and Wildlife 4: 295–300, http://dx.doi.org/10.1016/j.ijppaw.2015.05.004 Nelson FBL, Brown GP, Shilton C, Shine R (2015b) Host–parasite interactions during a biological invasion: The fate of lungworms (Rhabdias spp.) inside native and novel anuran hosts. International Journal for Parasitology: Parasites and Wildlife 4: 206–215, http://dx.doi.org/10.1016/j.ijppaw.2015.04.001 Özer A (2007) Metazoan parasite fauna of the round goby Neogobius melanostomus Pallas, 1811 (Perciformes: Gobiidae) collected from the Black Sea coast at Sinop, Turkey. Journal of Natural History 41:483–492, http://dx.doi.org/10.1080/00222930701234361 Paterson RA, Lal A, Dale M, Townsend CR, Poulin R, Tompkins DM (2013) Relative competence of native and exotic fish hosts for two generalist native trematodes. International Journal for Parasitology: Parasites and Wildlife 2: 136–143, http://dx.doi. org/10.1016/j.ijppaw.2013.03.004 Paterson RA, Townsend CR, Poulin R, Tompkins DM (2011) Introduced brown trout alter native acanthocephalan infections in native fish. Journal of Animal Ecology 80: 990–998, http://dx.doi.org/10.1111/j.1365-2656.2011.01834.x Paterson RA, Townsend CR, Tompkins DM, Poulin R (2012) Ecological determinants of parasite acquisition by exotic fish species. Oikos 121: 1889–1895, http://dx.doi.org/10.1111/j.16000706.2012.20143.x Poulin R, Paterson RA, Townsend CR, Tompkins DM, Kelly DW (2011) Biological invasions and the dynamics of endemic diseases in freshwater ecosystems. Freshwater Biology 56: 676– 688, http://dx.doi.org/10.1111/j.1365-2427.2010.02425.x Reyjol Y, Brodeur P, Mailhot Y, Mingelbier M, Dumont P (2010) Do native predators feed on non-native prey? The case of round goby in a fluvial piscivorous fish assemblage. Journal of Great Lakes Research 36: 618–624, http://dx.doi.org/10.1016/j.jglr.2010. 09.006 Ricker WW (1975) Computation and interpretation of biological statistics of fish populations. Bulletin of the Fisheries Research Board of Canada 191: 1–382 Sheath DJ, Williams CF, Reading AJ, Britton JR (2015) Parasites of non-native freshwater fishes introduced into England and Wales suggest enemy release and parasite acquisition. Biological Invasions 17: 2235–2246, http://dx.doi.org/10.1007/s10530-0150857-8 Sitjà-Bobadilla A (2008) Living off a fish: A trade-off between parasites and the immune system. Fish and Shellfish Immunology 25: 358–372, http://dx.doi.org/10.1016/j.fsi.2008.03.018 Taraschewski H (2006) Hosts and parasites as aliens. Journal of Helminthology 80: 99–128, http://dx.doi.org/10.1079/JOH2006364 Telfer S, Bown KJ, Sekules R, Begon M, Hayden T, Birtles R (2005) Disruption of a host-parasite system following the introduction of an exotic host species. Parasitology 130: 661–668, http://dx.doi.org/10.1017/S0031182005007250 Thieltges DW, Reise K, Prinz K, Jensen KT (2008) Invaders interfere with native parasite–host interactions. Biological Invasions 11: 1421–1429, http://dx.doi.org/10.1007/s10530-008-9350-y Thilakaratne IDSIP, McLaughlin JD, Marcogliese DJ (2007) Effects of pollution and parasites on biomarkers of fish health in spottail shiners Notropis hudsonius (Clinton). Journal of Fish Biology 71: 519–538, http://dx.doi.org/10.1111/j.1095-8649.2007.01511.x Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Frontiers in Ecology and the Environment 2: 183–190, http://dx.doi.org/10.1890/1540-9295(2004)002 [0183:PPAIBP]2.0.CO;2 Uglem GL, Larson OR (1969) The life history and larval development of Neoechinorhynchus saginatus Van Cleave and Bangham, 1949 (Acanthocephala: Neoechinorhynchidae). Journal of Parasitology 55: 1212–1217, http://dx.doi.org/10.2307/3277260 Walkey M (1967) The ecology of Neoechinorhynchus rutili (Müller). Journal of Parasitology 53: 795–804, http://dx.doi.org/ 10.2307/3276774 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