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Hierarchical taxonomic tree for all currently known hosts (n = 14) of Sphaerothecum destruens. A: Oncorhynchus tshawytscha (Chinook salmon), B: O. kisutch (Coho salmon), C: O. mykiss (rainbow trout), D: Salmo trutta (brown trout), and E: S. salar (Atlantic salmon) The Cyprinidae is represented by seven species belonging to seven genera; F: Cyprinus carpio (carp), G: Rutilus rutilus (roach), H: Abramis brama (bream), J: Leucaspius delineatus (sunbleak); K: Squalius fellowesii. In the calculation of host specificity, the species Pseudorabora parva (topmouth gudgeon; Family Cyprinidae), the species Oxynoemachelius sp. (Family Nemacheilidae) and Lepomis gibbosus (Family Centrachidae) were also included. The host specificity (STD) was calculated to be 3·82 with a variance of 0·49.
Source publication
The rosette agent
Sphaerothecum destruens
is a novel pathogen, which is currently believed to have been introduced into Europe along with the introduction of the invasive fish topmouth gudgeon
Pseudorasbora parva
(Temminck & Schlegel, 1846). Its close association with
P. parva
and its wide host species range and associated host mortalities, highlig...
Context in source publication
Context 1
... tree representing the taxonomic hierarchy of S. destruens host species was constructed (Fig. 1) using the Linnean classification and the specificity index (STD) for S. destruens was calculated to be 3·21 with a variance in taxonomic distinctness (VarSTD) of 0·49; supporting the generalist nature of S. ...
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... Furthermore, wetland ecosystems often harbour invasive species (Glińska-Lewczuk et al. 2016) and many freshwater fish species which have adapted to these conditions are at risk of severe decline (Sayer et al. 2011;Van Wichelen et al. 2022). Interaction with invasive species can cause various changes for native fish populations, such as a reduction in growth and recruitment (Tapkir et al. 2022), a change in isotopic niche position (Declerck et al. 2002;Busst and Britton 2017), increased predation rates (Reshetnikov 2003), enhanced disease transmission (Andreou and Gozlan 2016) or habitat displacement (Šmejkal et al. 2023a). All of these effects can lead to a reduction or extinction of the population of native species. ...
... However, an organism's niche consists of many different aspects of resource sharing in space and time (Schoener 1974;Jackson et al. 2011) and, thus, the insight into interspecific interactions is simplified by the approach used. Additionally, the negative impact of topmouth gudgeon on other fish species is specific due to the transmission of the rosette pathogen Sphaerothecum destruens, which has a negative impact on other native floodplain species, such as the sunbleak (Leucaspius delineatus) (Gozlan et al. 2005;Spikmans et al. 2020) and other fish species (Andreou and Gozlan 2016;Spikmans et al. 2020). The sunbleak is also classified as critically endangered in Czechia and the number of known populations is even lower than that of the crucian carp (Chobot and Němec 2017). ...
Invasive species pose a major threat to natural ecosystems and directly outcompete many native species, placing them at imminent threat of extinction. The topmouth gudgeon (Pseudorasbora parva) is on the EU’s blacklist of invasive freshwater species and threatens biodiversity, especially in wetland and floodplain ecosystems, aquacultures and village ponds. The crucian carp (Carassius carassius) is native to Europe and its populations have declined in large part of its native range, with invasive gibel carp (C. gibelio) suspected as a major cause of its decline. Invasions by topmouth gudgeon have been implicated in the decline of crucian carp populations but this still needs to be verified. The aim of this study was to evaluate by the experimental approach the competitive interaction between the two species, topmouth gudgeon and crucian carp, focusing on isotopic niche sizes and their overlap in syntopy. A four-month mesocosm experiment was performed to determine the isotopic niche of crucian carp and topmouth gudgeon living alone and in syntopy. Additionally, stable isotope data were collected at the sites where the two species co-occur to compare niche sizes and overlaps. Experimental data showed that the isotopic space of topmouth gudgeon responded more flexibly (reducing niche size at syntopy) than that of the crucian carp and confirmed a high isotopic niche overlap between the species. Field studies have shown that topmouth gudgeon has invaded the isotopic niche of the crucian carp, especially when another invasive species, the gibel carp, lived in the community (25% at 40% ellipse area and 50% at 95% ellipse area). When only the topmouth gudgeon and crucian carp were present in the field, the overlap was lower (3% and 48%, respectively) and directional overlap modelling showed that the crucian carp was more likely to invade the isotopic niche of topmouth gudgeon than vice versa. The data indicated that competition between crucian carp and topmouth gudgeon is likely, especially in syntopy with other invasive species. This study shows that the feeding plasticity of topmouth gudgeon likely facilitates its establishment outside its native range and, due to high isotopic niche overlap, threatens native fish with similar feeding ecology with competitive displacement.
... The topmouth gudgeon presents some life-history traits favoring its invasiveness: early maturity, high fecundity, rapid growth, and longevity (Gozlan et al., 2010. Where introduced, this species exerts multiple impacts, being a carrier for pathogens and parasites (Andreou & Gozlan, 2016;Combe & Gozlan, 2018;Gozlan et al., 2010;Spikmans et al., 2020) and competing for food with either native Declerck et al., 2002) or other alien fishes. Also, due to their high consumption of zooplankton and the subsequent increase in phytoplankton, this species accelerates the eutrophication of water courses (Adámek & Sukop, 2000a). ...
The topmouth gudgeon Pseudorasbora parva is one of the worst invasive species worldwide and is considered to be highly plastic in terms of its phenotype but also behavioral ecology. Here, we analyzed the population structure and the morphological and dietary plasticity of four populations of P. parva across the four seasons within the Arno River basin in Central Italy. We found that the studied populations were morphologically different, suggesting multiple introductions or adaptation to different environmental conditions. In all populations, males were bigger and, overall, more frequent than females. The gonadosomatic index showed a similar pattern across all populations, with higher spring and summer values, indicating a long reproductive period. The diet of P. parva considerably varied across populations and seasons, suggesting a high degree of spatio‐temporal trophic plasticity. Diet breadth varied among seasons, being more specialized in spring and summer and more opportunistic during autumn and winter. Our results highlight high trophic plasticity in the invasive populations of P. parva , potentially impacting multiple native taxa.
... The influence of native populations' genetic history on the reconstruction of invasion routes:… diversity to drive adaptation to the new environment (Roman and Darling 2007). A major biodiversity problem associated with P. parva is the fungus-like pathogen, the rosette agent Sphaerothecum destruens, for which it acts as a vector, and that has subsequently spread to invaded areas causing mortality in a large number of native freshwater fish species in Europe (Andreou and Gozlan 2016;Combe and Gozlan 2018). ...
... Furthermore, the co-introduction of non-native host-pathogen systems such as P. parva-S. destruens may create new host-pathogen interactions that can be detrimental to naïve native host species, hence providing a competitive advantage for the invaders (Price et al. 1986;Andreou and Gozlan 2016;Combe and Gozlan 2018;Vilcinskas and Knoll 2015). The gene flow resulting from the multiple introductions highlighted in Western Europe largely increased the effective population size as well as genetic diversity. ...
Insufficient data on the origins of the first introduced propagule and the initial stages of invasion complicate the reconstruction of a species’ invasion history. Phylogeography of the native area profoundly shapes the genomic patterns of the propagules on which subsequent demographic processes of the invasion are based. Thus, a better understanding of this aspect helps to disentangle native and invasive histories. Here, we used genomic data together with clustering methods, explicit admixture tests combined with ABC models and Machine Learning algorithms, to compare patterns of genetic structure and gene flow of native and introduced populations, and infer the most likely invasion pathways of the highly invasive freshwater fish Pseudorasbora parva. This species is the vector of a novel lethal fungal-like pathogen (Sphaerothecum destruens) that is responsible for the decline of several fish species in Europe. We found that the current genetic structuring in the native range of P. parva has been shaped by waves of gene flow from populations in southern and northern China. Furthermore, our results strongly suggest that the genetic diversity of invasive populations results from recurrent global invasion pathways of admixed native populations. Our study also illustrates how the combination of admixture tests, ABC and Machine Learning can be used to detect high-resolution demographic signatures and reconstruct an integrative biological invasion history.
... None of the parasites of topmouth gudgeon occurring in its native range, have been reported in Western Europe yet (Gozlan et al., 2010). However, most studies focus on topmouth gudgeon as a carrier of the intracellular parasite Sphaerothecum destruens Arkush, Mendoza, Adkison & Hedrick, 2003 (e.g., Andreou et al., 2011;Andreou & Gozlan, 2016;Spikmans et al., 2020) and none have performed a community-level analysis in the invasive range of the host. ...
Understanding why certain host species harbor more parasites is an important question in parasite and fish ecology. Parasite infection among sympatric species may integrate various processes affecting parasite assembly, including the species-specific ecology and the success of invaders. We focused on spatial, environmental, and host-related determinants of parasite assembly in three riverine fish species: the native three-spined stickleback and stone loach, and the invasive topmouth gudgeon. Parasite community structure differed significantly between the three host species. Three-spined stickleback harbored the most ectoparasites. Host density and nutrients were the strongest predictors of its parasite communities. Topmouth gudgeon harbored the lowest number of parasites, both in terms of abundance and species richness. None of the parasites identified originated from its expanded range, suggesting that enemy release occurred during invasion. Temperature and host density predicted parasite assemblages of topmouth gudgeon. Stone loach hosted the most endoparasites, likely resulting from its varied diet, benthic lifestyle, and larger size. Additionally, host size and condition were positively correlated with parasite infection, which was similar among the three host species. The results suggest that host-related factors have a similar effect among host species, while the importance of environmental and spatial factors differs according to host ecology.
... A major biodiversity concern associated with P. parva is the fungi-like Rosette Agent Sphaerothecum destruens , for which it acts as a healthy carrier that has subsequently spread into invaded areas and in many naïve native host species. This novel pathogen is a lethal intracellular pathogen responsible for the mortality of a large number of European native freshwater fish species (Andreou & Gozlan, 2016;Combe & Gozlan, 2018). ...
Invasive species are significant contributors to global changes and constitute a severe threat to biodiversity. Yet invasions offer an incredible framework to understand how small and low-diverse introduced populations adapt to novel environmental conditions and succeed in colonizing large areas. However, due to the insufficient data on the origin of the first introduced propagule and the first stage of invasion, reconstructing a species’ invasion history is challenging. Here, we applied genetic clustering methods and explicit admixture tests combined with ABC models and Machine Learning algorithms to describe the phylogeography of native and invasive populations and infer the most probable demographic invasion scenarios of Pseudorasbora parva, a highly invasive freshwater fish and the healthy carrier of a novel lethal fungi-like pathogen (Sphaerothecum destruens), which is responsible for the decline of several fish species in Europe. We found that the current genetic structuring of the native P. parva range has been shaped by waves of gene flow originating from southern and northern Chinese populations. Furthermore, our results strongly suggest that the invasive genetic diversity is the outcome of past recurrent global invasion pathways of admixed native populations. Our study also illustrates how the combination of admixture tests, ABC, Machine Learning can be used to detect high-resolution demographic signatures and reconstruct an integrative biological invasion history.
... High densities of P. parva have severe and significant impacts on native trophic food webs, resulting in overlaps with native fishes trophic niche . Additional concerns include egg predation, hybridisation with endemic and rare species (Gozlan & Beyer, 2006;Konishi et al., 2003;Simon et al., 2011), facultative parasitism (Gozlan, Andreou, et al., 2010), and transmission of diseases such as the rosette agent Sphaerothecum destruens, which is a novel fungal fish pathogen responsible for the decline of many native fish populations (Andreou & Gozlan, 2016;Combe & Gozlan, 2018;Spikmans et al., 2020). ...
1. Iran is a major freshwater fish diversity hotspot in the Middle East, and is an important
zoogeographical area in west Asia, acting as the crossroads and dispersal
corridor between several major biogeographical realms of the world. The topmouth
gudgeon, Pseudorasbora parva was first recorded in Iran on 6 May 1991 in
the Caspian Sea basin and is now widely distributed across the country. Despite
widespread distribution in the Iranian inland waters, its invasion history and genetic
background remain unknown.
2. Here, based on the mitochondrial DNA control region (806 bp) sequence variation
of 161 P. parva samples collected from 15 Iranian localities and additional sites in
Europe and Asia, as well as a cytochrome c oxidase subunit I barcode database
(615 bp) including 166 novel and archived sequences, we characterised the pattern
of genetic diversity and its colonisation history in Iran.
3. Our results show the presence of three matrilineal haplotypes in Iran belonging
to two distinct lineages: (1) a widespread lineage with a common haplotype found
throughout the country and one exclusive haplotype confined to the Mashkid
basin, whose origin can be traced back to a single introduction of a small number
of propagules from Japan and corresponded to the Iranian introduction of P. parva
in the late 1980s; (2) a Chinese lineage represented by a single haplotype found in
the Shafarood River of the Caspian Sea basin but also translocated to central Iran,
penetrated recently to northern Iran through natural dispersal from Azerbaijan as
an extension of the European wave of invasion.
4. At the global scale, there is less genetic diversity in west Asia than in Europe
and the Asian native range. At the local scale, estimates of genetic diversity in
Iranian P. parva populations are extremely low but the Caspian Sea and Esfahan
basins gained higher diversities from admixture of highly divergent Japanese and
Chinese lineages. Our phylogenetic and species delimitation analyses also suggest
the existence of multiple putative species in the native range of P. parva and stress
the need of an integrative taxonomical approach based on additional morphological
and nuclear DNA data.
... This species was accidently translocated together with the voluntary spread of Asian carp species for fish farming and consequently spread (Gozlan et al., 2010). Despite its preference for lotic systems where it generally reaches high abundances, it shows wide environmental adaptability (Britton et al., 2008;Yan & Chen, 2009), being a carrier for pathogens and parasites (Andreou & Gozlan, 2016;Combe & Gozlan, 2018;Gozlan et al., 2010;Spikmans et al., 2020) and competing for food with native fishes Declerck et al., 2002). The common bleak Alburnus alburnus (Linnaeus 1758) is native to Europe, north of Caucasus, Pyrénées and the Alps, eastward to Ural and Emba, while not being native to southern Europe (Amat-Trigo et al., 2019). ...
Invasive fish species impact aquatic ecosystems and modify native communities, often leading to a decline in local species. These ecological impacts include the transmission of pathogens, predation, competition as well as hybridization. Two invasive fish species, the common bleak Alburnus alburnus and the topmouth gudgeon Pseudorabora parva, have both been recently found co‐occurring in several regions of southern Europe, such as the Italian Arno River. Nonetheless, the trophic relationships among invasive fish species, especially cyprinids, remain poorly understood, and no studies have reported the trophic interaction between these two species. This study compared length–weight relationship and used stomach content and stable isotope analysis of two co‐occurring populations in the Arno River to characterize the growth and overlap of potential trophic niches. It also found similar allometric growth in both species, a wider generalist trophic niche for P. parva and a more specialized niche for A. alburnus. A considerable niche overlap was found, suggesting that feeding competition can occur if resources were to be limited. Moreover, the niche of P. parva was more likely to overlap with that of A. alburnus than vice versa, suggesting that P. parva can be considered as a potential over competitor. Nonetheless, the authors found in the overlapping populations no evidence of realized competition, probably avoided through a combination of fine‐scale mechanisms. They also highlighted that these two invasive species can co‐exist and share resources, at least in an open ecosystem like a river, thus potentially doubling up their trophic impact on local communities.
... Background Introduced parasites can cause significant population declines in susceptible species and generalist parasites in particular, are more likely to be introduced, established and expand their host range [1,2]. The eukaryotic parasite Sphaerothecum destruens is considered a true generalist [1] that can infect and cause high mortalities in freshwater fish species; including commercially important species such as carp and Atlantic salmon [3,4]. ...
... Background Introduced parasites can cause significant population declines in susceptible species and generalist parasites in particular, are more likely to be introduced, established and expand their host range [1,2]. The eukaryotic parasite Sphaerothecum destruens is considered a true generalist [1] that can infect and cause high mortalities in freshwater fish species; including commercially important species such as carp and Atlantic salmon [3,4]. Sphaerothecum destruens has been recorded in North America [5][6][7], Europe [8][9][10][11][12] and China [10]. ...
Background:
Sphaerothecum destruens is an obligate intracellular fish parasite which has been identified as a serious threat to freshwater fishes. Taxonomically, S. destruens belongs to the order Dermocystida within the class Ichthyosporea (formerly referred to as Mesomycetozoea), which sits at the animal-fungal boundary. Mitochondrial DNA (mtDNA) sequences can be valuable genetic markers for species detection and are increasingly used in environmental DNA (eDNA) based species detection. Furthermore, mtDNA sequences can be used in epidemiological studies by informing detection, strain identification and geographical spread.
Methods:
We amplified the entire mitochondrial (mt) genome of S. destruens in two overlapping long fragments using primers designed based on the cox1, cob and nad5 partial sequences. The mt-genome architecture of S. destruens was then compared to close relatives to gain insights into its evolution.
Results:
The complete mt-genome of Sphaerothecum destruens is 23,939 bp in length and consists of 47 genes including 21 protein-coding genes, 2 rRNA, 22 tRNA and two unidentified open reading frames. The mitochondrial genome of S. destruens is intronless and compact with a few intergenic regions and includes genes that are often missing from animal and fungal mt-genomes, such as, the four ribosomal proteins (small subunit rps13 and 14; large subunit rpl2 and 16), tatC (twin-arginine translocase component C), and ccmC and ccmF (cytochrome c maturation protein ccmC and heme lyase).
Conclusions:
We present the first mt-genome of S. destruens which also represents the first mt-genome for the order Dermocystida. The availability of the mt-genome can assist the detection of S. destruens and closely related parasites in eukaryotic diversity surveys using eDNA and assist epidemiological studies by improving molecular detection and tracking the parasite's spread. Furthermore, as the only representative of the order Dermocystida, its mt-genome can be used in the study of mitochondrial evolution of the unicellular relatives of animals.
... Many closely related human pathogens from the Onygenales order, such as Blastomyces, Emmonsia, Paracoccidioides, and Histoplasma, also have been isolated from a wide variety of animals (wild mice, bats, birds, armadillos, etc.) and have the ability to cause devastating mycoses in humans [47][48][49][50][51][52]57]. A generalist pathogen can infect a wide variety of host species with varying severities, and the host range of the pathogen is determined by the physiological, behavioral and ecological characteristics of the host that determines the ability of a pathogen to infect the host and complete its lifecycle [58][59][60]. The data show that a variety of animal species are associated with burrows where Coccidioides posadasii is prevalent in Arizona. ...
The lack of knowledge regarding the ecology of Coccidioides spp. makes both modeling the potential for disease outbreaks and predicting the distribution of the organism in the environment challenging. No single ecological parameter explains the biogeography of the pathogen. Previous investigations suggest an association with desert mammals, but these results should be confirmed with modern molecular techniques. Therefore, we used molecular tools to analyze soils associated with animal activity (i.e., burrows) to better define the ecology and biogeography of Coccidioides spp. in Arizona. Soils were collected from locations predicted to have favorable habitat outside of the established endemic regions to better understand the ecological niche of the organism in this state. Our central hypothesis is that soils taken from within animal burrows will have a higher abundance of Coccidioides spp. when compared to soils not directly associated with animal burrows. Our results show that there is a positive relationship with Coccidioides spp. and animal burrows. The organism was detected in two locations in northern Arizona at sites not known previously to harbor the fungus. Moreover, this fungus is able to grow on keratinized tissues (i.e., horse hair). These results provide additional evidence that there is a relationship between Coccidioides spp. and desert animals, which sheds new light on Coccidioides’ ecological niche. These results also provide evidence that the geographic range of the organism may be larger than previously thought, and the concept of endemicity should be reevaluated for Coccidioides.
... Threats caused by alien pathogens, often associated with other invasive species that serve as reservoirs, are poorly understood and deserve more attention in risk assessment and management of biological invasions (Roy et al. 2017). Pathogen pollution caused by spill-over from invasive fish species goes largely undetected in ongoing monitoring schemes, clouding the causes of their detrimental effects on naïve native species (Andreou and Gozlan 2016). ...
... Sphaerothecum destruens is a generalist and known to have a broad host species spectrum (Arkush et al. 2003;Gozlan et al. 2009;Andreou et al. 2012;Andreou and Gozlan 2016) and it is being found in an increasing number of fish species in wild populations: Oncorhynchus tshawytscha, Oncorhynchus kisutch (Arkush et al. 1998), P. parva (Gozlan et al. 2005), L. delineatus (Andreou et al. 2011), Dicentrarchus labrax, Lepomis gibbosus, Oxynoemacheilus sp., Petroleuciscus smyrnaeus, Squalius fellowesii (Ercan et al. 2015), Leuciscus leuciscus, Rutilus rutilus, Squalius cephalus and Salmo trutta (Sana et al. 2018). In experimental or hatchery conditions, several other fish species have proven to act as hosts: Oncorhynchus mykiss (Arkush et al. 1998), Salmo salar (Paley et al. 2012), A. brama and C. carpio . ...
... Effects of both P. parva and S. destruens easily go undetected (Andreou and Gozlan 2016). Ongoing monitoring programmes for ecological status assessments of water systems according to the EU Water Framework Directive, conservation status of protected areas according to the EU Habitat Directive and the Dutch national long-term fish monitoring programme (De Graaf et al. 2016) are unable to detect declines of native fish associated with P. parva or S. destruens. ...
The Asian cyprinid Pseudorasbora parva is considered to be a major threat to native fish communities and listed as an invasive alien species of European Union concern. Our study aims to gain evidence-based knowledge on the impact of both P. parva and its parasite Sphaerothecum destruens on native fish populations by analysing fish assemblages and body condition of individuals of native fish species in floodplain water bodies that were invaded and uninvaded by P. parva. We explored the use of environmental DNA (eDNA) techniques to detect S. destruens. Prevalence of S. destruens in native fish species was assessed. Fish samplings showed significantly negative correlations between the abundance of P. parva and the native Leucaspius delineatus, and Pungitius pungitius and three biodiversity indices of the fish assemblages (Simpson’s diversity index, Shannon–Wiener index and evenness). Contrastingly, the abundances of the native Gasterosteus aculeatus and P. parva were positively related. In nearly all isolated water bodies with P. parva, this species is outnumbering native fish species. No effect of P. parva presence was found on body condition of native fish species. Sphaerothecum destruens was demonstrated to occur in both P. parva and G. aculeatus. Gasterosteus aculeatus is suggested to be an asymptomatic carrier that can aid the further spread of S. destruens. Analysis of eDNA proved to be a promising method for early detection of S. destruens, here showing that S. destruens presence coincided with P. parva presence. The ongoing invasion of both P. parva and S. destruens is predicted to pose a significant risk to native fish communities.
