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All issues No 424 (2023) Knowl. Manag. Aquat. Ecosyst., 424 (2023) 9 Full HTML
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Knowl. Manag. Aquat. Ecosyst.
Number 424, 2023
Anthropogenic impact on freshwater habitats, communities and ecosystem functioning
Article Number 9
Number of page(s) 12
DOI https://doi.org/10.1051/kmae/2023006
Published online 05 April 2023

© H. Ahnelt et al., Published by EDP Sciences 2023

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (https://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material.

1 Introduction

The unusual life cycle of freshwater mussels (Bivalvia, Unionida) is characterized by a close link to freshwater fishes via a temporary but obligatory parasitic stage. Specialized larvae, the glochidia, are able to attach on the external surface on various body parts and fins, where they encyst and metamorphose to free-living juvenile mussels (Kat, 1984; Douda et al., 2012; Modesto et al., 2018). Many, but not all, freshwater mussels are host generalists in so far as their glochidia can attach to various fish species (Haag and Warren, 1997; 2003; Douda et al., 2012). Nevertheless, not all of these fish species are suitable as hosts. Some species are merely marginally suitable because only few glochidia can transform into juvenile mussels (Haag and Warren, 1997; summarized in Modesto et al., 2018) or complete development into juveniles is unsuccessful, for example due to an immune response of the fish host (Reuling, 1919; Jansen et al., 2001; Ieshko et al., 2016).

Altered fish host behavior due to glochidia infestation such as reduced migration behavior was described by Horky et al. (2014). Conversely, host behavior may affect the probability of the glochidia to attach. Glochidia of many mussel species sink to the ground after being released. Benthic and epibenthic fishes at or close to the bottom of a water body are more likely to become parasitized by these glochidia than pelagic fishes (McMahon and Bogan, 2001). The few studies on the pattern of glochidia attachment to the host showed that they do not attach randomly, but that certain body regions are more affected than others (Giusti et al., 1975; Dartnall and Walkey, 1979; Dudgeon and Morton, 1984; Martel and Lauzon-Guay, 2005).

So far, a recent review has reported 326 fish host species for unionids (Modesto et al., 2018). Although gobioid fishes are adapted to a benthic life style, world-wide only eight of these species (2.5%) were listed as hosts in that review. Gobioid males are generally territorial, construct and guard nests. During these activities and when eggs and larvae are fanned with fresh water, glochidia find ideal conditions for contact. Such a ‘glochidia friendly’ behavior was already mentioned by Watters (1994) for Centrarchidae (sunfishes), which also construct and guard nests.

Lake Trasimeno, the fourth largest freshwater lake in Italy (Giardino et al., 2010; Lorenzoni et al., 2010), was variously altered by anthropogenic activities (Giusti et al., 1975; Mearelli et al., 1990; Ludovisi and Gaino, 2010; Carosi et al., 2019). This included numerous fish introductions (Lorenzoni et al., 2006, 2010). Seventy-four percent of the 19 species documented for the lake are introduced, a mere five are native (Lorenzoni et al., 2015; Carosi et al., 2019). Two gobies of the ‘sand goby’ group were likely accidentally introduced with fish fry, namely Knipowitschia panizzae (Berg 1916) and Pomatoschistus canestrinii (Ninni 1883), both endemic to the Adriatic catchment. Today, these two sand gobies are acclimated and abundant in the lake (Ahnelt et al., 2018).

Currently, four mussel species of the tribe Anodontini are documented for the lake. Three of them are native, the Duck mussel Anodonta anatina (Linnaeus 1758), the Swan mussel A. cygnea (Linnaeus 1758) and the Fretted mussel A. exulcerata Porro 1838, and one is introduced, the Chinese pond mussel Sinanodonta woodiana (Lea 1834) (Froufe et al., 2017). Back in the 1970s, the development of a freshwater mussel and of the glochidia in Lake Trasimeno was already documented (Giusti et al., 1975). Those authors, however, assumed that the lake was inhabited by only a single Anodonta species, A. cygnea. The authors based their study on extensive samples from three localities of the lake, and their analysis of the glochidia was likely a mix of more than one species, possibly of all three anodontin mussels (S. woodiana was first detected in Italy in 1996 (Maganelli et al., 1998)). World-wide not only populations of freshwater mussels but also populations of many freshwater fishes, hosts of the parasitic stage of the mussels, are declining (Modesto et al., 2018). The loss of host fish availability can have severe effects on freshwater mussel dispersion and thus on the status of their populations (Schwalb et al., 2011; Douda et al., 2012; Froufe et al., 2014) in the worst case resulting in extinction cascades (Modesto et al., 2018). Recently, it has been shown that glochidia of freshwater mussels also attach to gobioid species of Ponto-Caspian origin which are exotic in Central and Western Europe (Ondračková et al., 2005; 2009; Antal et al., 2015; Šlapansky et al., 2016). Such introduced species may have severe effects on freshwater mussel populations in two ways. They could be beneficial as new hosts but may also act as a sink if the attached glochidia cannot develop to young mussels (Šlapansky et al., 2016; Tremblay et al., 2016).

In this study we report (1) the first infestation of Gobioidei with glochidia of freshwater mussels in the wild in Europe outside the Ponto-Caspian region, (2) two Gobionellidae (‘gobies’ in the following) endemic to the Adriatic basin as new hosts for glochidia, (3) the infestation of these two gobies by only a single anodontin species and (4) the topography of glochidia attachment on these two hosts. We also present an extensive literature survey on gobioid fishes as hosts of the parasitic stage of freshwater mussels world-wide.

2 Materials and methods

2.1 Study area

Lake Trasimeno (43°06′ N, 12°07′ E) measures 124 km2, making it the fourth largest lake in Italy. It is shallow (average depth: 4.7 m; max. depth: 6.3 m), has no thermal stratification, the water transparency is low and the water temperature is about the same as the air temperature (Giardino et al., 2010; Lorenzoni et al., 2010; Ludovisi and Gaino, 2010; Carosi et al., 2019). Nineteen fish species occur in the lake, most of them accidently introduced for fishing purposes. The fish fauna is dominated by cyprinid fishes such as goldfish (Carassius sp.), rudd (Scardinius hesperidicus Bonaparte, 1845) and the tench (Tinca tinca (Linnaeus, 1758)) (Lorenzoni et al., 2010).

From 3 March 2022 to 24 May 2022, five samplings were conducted on the east shore of the lake, at “Monte del Lago” (43° 8.797′ N; 12° 9.887′ E) (Fig.1A). The site is located in a shallow pebbly bottom area (Fig. 1B), in a littoral stretch free from the presence of Phargmites australis (Cav.) Trin. ex Steud. 1840, which, however, is abundant in the surrounding areas.

thumbnail Fig. 1

A: map of Italy showing location of Lake Trasimeno and location of sampling site (red dot). B: sampling site at Monte del Lago. Photo A. Carosi.

2.2 Material

2.2.1 Fishes

Sand gobies of the genera Knipowitschia and Pomatoschistus have a benthic life-style, are opportunistic feeders predating mostly on macroinvertebrates, and prefer soft bottoms (Miller, 2004). We investigated a total of 148 sympatrically occurring gobies: 62 specimens of the Adriatic dwarf goby Knipowitschia panizzae and 86 specimens of the Canestrini's goby Pomatoschistus canestrinii. The sex was determined based on the shape of the urogenital papilla, longer than wide and tapering in males, shorter and about as long as wide in females. Fishes were sampled with the permission of the state and regional institutions and were in accordance with Italian state laws on fisheries.

The systematics of the Gobioidei (as suborder of Gobiiformes) is still in progress. Therefore, we keep the Gobionellidae sensu Thacker (2009) on family level.

2.2.2 Mussels

Four species of Unionidae are documented for Lake Trasimeno, three native (Anodonta anatina, A. cygnea, A. exulcerata) and one non-native (Sinanodonta woodiana) (Froufe et al., 2017; Riccardi et al., 2020). Only two of these four unionid mussel species were present at the sampling locality of the gobiid fishes, the Duck mussel Anodonta anatina and the Chinese pond mussel Sinanodonta woodiana.

We investigated shells of a total of 12 mussels, eight Anodonta anatina and four Sinanodonta woodiana. These two species were distinguished based on their different umbonal sculpture. The umbonal ridges of A. anatina characteristically crossed the growth ridges, whereas those of S. woodiana were more elevated and further apart than those of A. anatina. Additionally, A. anatina has more elongated, rhombic shells, with the dorsal margin slightly bent and the lower edge characteristically thickened. In contrast, the shells of S. woodiana were more roundish, nearly circular.

Genetic data were retrieved from nine glochidia, five from K. panizzae and four from P. canestrinii.

2.3 Methods

The fishes were sampled along the shore of the lake by electrofishing, using a direct electric current with a power of 4,500 W. Specimens were euthanized by an overdose of phenoxyethanol and preserved in 99.8% ethanol.

The gobies were examined for the presence of parasites using a stereo microscope. The attachment sites of glochidia were individually documented for each specimen. The recorded attachment sites were grouped into fins, head, trunk and tail (from anus to base of caudal fin) for a total of nine attachment sites (Tab. 1). We did not differentiate between left and right side but summarized these data. To test if glochidia were attached on gills, nine of the largest infested specimens and six of the largest specimens without external glochidia infestation were examined.

Glochidia for genetic analysis were dissected from their cysts with aid of insect needles: four such glochidia from P. canestrinii and five from K. panizzae. DNA was extracted using the whole specimen with the Qiagen's DNA MicroKit following the associated protocol and elution in 25 μl elution buffer. The DNA concentration was measured with the Invitrogen Qubit Fluorometer from Thermo Fisher Scientific. The Qubit™ dsDNA HS Assay Kit with the associated standard protocol was used. To amplify the DNA barcoding fragment of the mitochondrial cytochrome oxidase 1 gene, the primer pair LCO1490_Mol1/HCO2198_Mol1 (Duda et al., 2017) was used. PCRs were performed on a Master Gradient thermocycler (Eppendorf) in 25 µl elution buffer with 5 µl template DNA, using the QIAGEN Multiplex PCR Kit with 0.5 µM of each primer. Each PCR comprised 40 reaction cycles with an annealing temperature of 50°C. Control reactions were carried out for both DNA extractions and PCR amplifications. PCR products were purified using the QIAquick PCR Purification kit (Qiagen) and analyzed by direct sequencing (both directions) by Microsynth Austria GmbH using the PCR primer pairs.

Four voucher specimens of both goby species infested with parasitic glochidia are deposited in the Collection Mollusca of the Natural History Museum of Vienna with the register numbers NHMW-MO-113654 (Knipowitschia panizzae) and NHMW-MO-113655 (Pomatoschistus canestrinii). Further specimens (infested or not infested) are deposited in the Ichthyological Collection of the Natural History Museum of Vienna with the register numbers NMW 100508–100509 (K. panizzae) and NMW 100510–100511(P. canestrinii). Shells of Anodonta anatina (NMHW-MO-113652) and Sinanadonta woodiana (NMW-MO-113653) are deposited in the Collection Mollusca of the Natural History Museum.

Giusti et al. (1975) gave inconsistent numbers regarding the infestation of fishes with glochidia in Lake Trasimeno. On page 105 (penultimate sentence), they mention that glochidia were found in 53% of L. gibbosus, 16.6% of T. tinca, 54.5% of P. fluviatilis and 37.5% of A. boyeri. From Fig. 7, page 106, about the same percentage is shown for P. fluviatilis, but much lower values are given for L. gibbosus (about 35%) and T. tinca (about 6%). Nevertheless, the exact number of individuals of fish species examined and how many of them were infested is listed on page 109, Fig. 9: L. gibbosus − examined 173 specimens of which 53 were infested 53, which equals 30.6%; T. tinca − examined 140, infested 39 (27.9%); P. fluviatilis − examined 615, 167 infested (27.2%) and A. boyeri − examined 99, infested 31 (31.3%). We therefore follow these data in Fig. 9 of Giusti et al. (1975) based on the exact number of examined vs. infested specimens.

Table 1

Knipowitschia panizzae and Pomatoschistus canestrinii from Lake Trasimeno; number (N) of specimens with glochidia of Anodonta anatina attached to different parts of the body in total and by sex. A = anal fin, C = caudal fin, D1, D2 = first and second dorsal fin, P = pectoral fins and V = pelvic fins (fused to pelvic disc).

2.3.1 Statistical analysis

A Fisher's Exact test was used to assess differences in the proportion of infested specimens between P. canestrinii and K. panizzae, and between sexes. The comparison of the mean number of attached glochidia between the two fish species, and between sexes, was performed using a t-test. A chi-square test was used to assess differences between the two species and between sexes in the proportion of attached glochidia for target body regions.

The between-sex comparison of the average number of glochidia detected in the various body parts was performed by MANOVA. All analyses were done using Dell STATISTICA 13 software.

3 Results

3.1 Infestation and topography of attachment

Glochidia-infected gobies were recorded during the sampling events in March and April. Specimens collected in May were parasite free.

We found that 51.4% (n = 76) of all sampled gobies (n = 148), collected on a single locality in Lake Trasimeno, had glochidia attached (Fig. 2). The maximum number per specimen was five for both P canestrinii and for K. panizzae. Nevertheless, the vast majority of specimens were infested by only 1–2 glochidia, 77.1% (n = 37) in P. canestrinii and 64.3% (n = 18) in K. panizzae; 3–5 glochidia were found in 22.9% (n = 11) of P. canestrinii and in 35.7% (n = 10) of K. panizzae (Tab. 2).

More P. canestrinii were affected (55.8%) (n = 48) than K. panizzae (45.2%) (n = 28) (Tab. 3), but this difference was not significant based on the Fisher's Exact test (p = 0.085). Nevertheless, in the mean (mean intensity of infestation), the glochidia burden was larger in K. panizzae (2.2 vs. 1.8); again, this difference was not significant (t-test: t = 2.97; p = 0.089). The largest mean number of attached glochidia occurred in female K. panizzae (3.9); males carried only 1.9. In P. canestrinii the respective values were 1.9 and 1.6, respectively (Tab. 4). The differences between the sexes are statistically significant for K. panizzae (t = 4.78; p = 0.038), but not for P. canestrinii (t = 1.09; p = 0.301). In both species, males were infested to a larger percentage than females (P. canestrinii 61.8% vs. 53.8%; K. panizzae 53% vs. 36.7%). This difference was more expressed in K. panizzae. However, in neither P. canestrinii (p = 0.507) nor in K. panizzae (p = 0.499) were the differences between the sexes statistically significant based on Fisher's Exact test. No glochidia were found on the gills (n = 15 for both species).

thumbnail Fig. 2

Glochidia of Anodonta anatina (black arrows) attached to hosts Pomatoschistus canestrinii (NHMW-MO-113655) (A, B) and Knipowitschia panizzae (NHMW-MO-113654) (C, D). Parasites attached to A: the pectoral and the pelvic fins (united to pelvic disc); B: same specimen, encysted glochidium, right pectoral fin; C: base of pectoral disc; D: same specimen, pectoral disc enlarged. Scale of A, C = 5 mm; scale of B, D = 1 mm. Photos C. Hörweg, H. Ahnelt.
Table 2

Knipowitschia panizzae and Pomatoschistus canestrinii from Lake Trasimeno; sampling dates from March − May 2022 with number of specimens in total and, in parentheses, females/males, of not infested and infested specimens.

Table 3

Fish species of Lake Trasimeno infested with glochidia of Anodonta anatina * (this study) and Anodonta sp.**. Ab = Atherina boyeri, Kp = Knipowitschia panizzae, Lg = Lepomis gibbosus, Pc = Pomatoschistus canestrinii, Pf = Perca fluviatilis, Tt = Tinca tinca.

Table 4

Percentage of glochidia attachment on the four most infested structures of Knipowitschia panizzae and Pomatoschistus canestrinii separated by species and, within species, by sex. C = caudal fin, P = pectoral fin and V = pelvic fin (sucking disc).

3.2 Pattern of attached glochidia

All nine investigated regions of both species combined were targets of glochidia, although none were found on the first dorsal fin, the trunk and the tail in K. panizzae (Tab. 1).

In the mean number of glochidia per specimen was 1.8 on P. canestrinii. Except for the two dorsal fins of the males, glochidia occurred on all nine investigated structures, but in different proportions (Tab. 1). Most affected were fins: pectoral fins 27.9% (n = 24), pelvic fins 22.1% (n = 19), caudal fin 23.3% (n = 20), anal fin 5.8% (n = 5), the head 15.1% (n = 13), the two dorsal fins 1.1% (n = 1) each, the trunk 1.1% (n = 1) and the tail 2.3% (n = 2). The differences between the frequencies were highly significant (chi-square test: χ2 = 68.87; p = 0.001).

The mean number of glochidia per specimen was 2.2 on K. panizzae. They occurred on seven of nine structures, and in different proportions. In this species the trunk and tail were not affected (Tab. 1). Most affected were fins: pectoral fins 32.3% (n = 20), pelvic fins 32.3% (n = 20), caudal fin 11.3% (n = 7), anal fin 4.8% (n = 3), first dorsal fin 3.2% (n = 2), second dorsal fin 1.6% (n = 1) and head 14.5% (n = 9). The differences between the percentage frequencies were highly significant (χ2 = 45.99; p = 0.001).

By far the most glochidia were attached to the fins of both species; in P. canestrinii 81.4% (n = 70) vs. 18.6% (n = 16) on the entire body (head, trunk, tail). In K. panizzae the corresponding values were 85.5% (n = 53) on the fins vs. 14.5% (n = 9) on the entire body (Tab. 4).

We found only encysted glochidia on the fishes (Fig. 2). We could not determine the metamorphosis rate and whether the glochidia metamorphosed into juveniles or remained encysted.

3.3 Temperature-dependent infestation

Water temperature increased during the sampling period (3 March–24 May) from 7 °C to 24.4 °C and during the period with attached glochidia (3 March–22 April) from 7 °C to 16.3 °C (Tab. 5). No temperature-dependent infestation gradient was recorded for either fish species.

Table 5

Infestation (mean number) of Knipowitschia panizzae and Pomatoschistus canestrinii with glochidia of Anodonta anatina and water temperature of Lake Trasimeno during sampling period. *April 22: only one, not infested, specimen of K. panizzae was collected.

3.4 Sexual dimorphism and glochidia infestation

Of the nine investigated morphological structures, some were differently infested in males and females of both fish species. This involved six structures in K. panizzae but only three of the nine structures in P. canestrinii (Tab. 4). The paired fins of male K. panizzae were more infested than those of the females (pectoral fin 40.6% vs. 23.3%, pelvic fins 37.5% vs. 27.7%); in contrast, we detected more glochidia on the head (23.3% vs. 6.3%), on the caudal fin and, to a lesser extent, on the anal fin (16.7% vs. 6.3%, 6.7% vs. 3.1%) in females than in males. In P. canestrinii the differences between sexes were distinct only on the caudal fin (males 29.4% vs. females 19.2%), on the head (females 17.3% vs. males 1.8%) and on the anal fin (females 7.7% vs. males 3.1%).

Despite a seeming trend to sexual bias of certain body regions in both species, statistical analysis did not support sexual dimorphism. The average number of glochidia on the various body parts of the two sexes were not statistically significant (MANOVA), neither for K. panizzae (F = 1.045, p = 0.411) nor for P. canestrinii (F = 0.756, p = 0.659).

3.5 Literature survey

The literature survey yielded 42 publications from 1991 and 2021 which reported 33 gobioid species as hosts of glochidia of unionid mussels world-wide. Documentations came from four continents and 17 countries: Australia, Japan, New Zealand, Thailand, USA and 12 in Europe (Tab. 6).

Somewhat more than the half of these records (17 of 33 = 51.5%) are based on laboratory experimental infestations; only 48.5% are based on records from the wild. Including K. panizzae and P. canestrinii of the present study, to date 33 gobioid species from four families − 4 Eleotridae, 20 Gobiidae, 7 Gobionellidae (= Oxudercidae) and 2 Odontobutidae − are known as (potential) hosts for freshwater mussels (Tab. 6).

Table 6

Literature survey of gobioid fishes infested with glochidia of Unionidae (Bivalvia: Unionida). Gobioidei infested with glochidia: n = 33 (Graf (1997), who just mentioned “goby”, is not included in this number). The eight species listed by Modesto et al. (2018) are shaded in grey. Note, that for each species/country just one publication, as example, is listed.

4 Discussion

We found a high prevalence (∼50%) of the obligatory, time-limited parasitic stage of the freshwater mussel A. anatina on two gobies, the Adriatic dwarf goby K. panizzae and the Canestrini's goby P. canestrinii. These small, short-lived fishes (± annual) (Miller, 2004) were accidentally introduced in Lake Trasimeno, where they established large populations (Borroni, 1976; Freyhof, 1998). No records of infestation of these gobies with glochidia in their natural distribution area are documented. Such a report involving an infestation by Anodonta sp. is available only for a congener of the Adriatic dwarf goby, the Caucasian dwarf goby K. caucasica (Berg 1916), introduced in Hungary (Antal et al., 2015).

Gobioid fishes are relatively rarely mentioned as hosts for glochidia of unionid mussels. Modesto et al. (2018) reported 326 fish host species, but only eight (2.5%) of them were gobioids. Our survey increased this number to 33 species (Tab. 6). Although the typically benthivorous gobioids now make up 9.4% of the known 351 fish host species, these fishes are relatively insignificant as potential hosts for freshwater mussels in species number. Note also that 17 of these 33 species, infestations are known only from laboratories (Tab. 6). This also includes Padogobius bonelli (Bonaparte 1846) (as P. martensii (Günther 1861)) from the Po River drainage area (northern Italy) (Nagel and Castagnolo, 1991). To our knowledge, no further record (either from the laboratory or the wild) of other gobioid host species is known from the Italian peninsula. The other gobioids reported from Europe as hosts for glochidia are all of Ponto-Caspian origin except for the Far East Asian Perccottus glenii Dybowski 1877. That species was introduced to the European part of Russia in the early 20th century and is currently spreading through eastern and central Europe (Reshentikov, 2013; Grabowska et al., 2020). This makes the two sand gobies K. panizzae and P. canestrinii the first gobioid fishes with natural glochidia infestation in the wild in Italy and Europe outside of the Ponto-Caspian region and the Danube River watershed, or which are not of Ponto-Caspian origin.

Anadontin mussels are generalists in that they use taxonomically widely different fish species as hosts, mostly cyprinids, but also salmonids, esocids, gasterosteids or centrarchids (e.g., Dartnall and Walkey, 1979; Patzner, 2004; Blažek and Gelnar, 2006; Douda et al., 2012; Lopes-Lima et al., 2017). Giusti et al. (1975) also found a series of fish species infected by anadontin glochidia. Those authors were the first to study this issue in Lake Trasimeno (central Italy), but assumed that only one anadontin mussel, A. cygnea, occurred in the lake. Based on our results, their analysis probably involved a mix of more than one, possibly of all three native anodontin mussels. Sinanodonta woodiana, the fourth anadontin mussel, was first documented for Italy in 1996 (Maganelli et al., 1998).

Giusti et al. (1975) reported relatively low infestation rates in Lake Trasimeno. About one quarter of Perca fluviatilis Linnaeus 1758 and T. tinca specimens, and only one third of E. cisalpinus Bianco and Delmastro 2011 (as E. lucius Linnaeus 1758) and of Lepomis gibbosus (Linnaeus 1758) specimens, carried glochidia (Table 3). We found glochidia on about half of the K. panizzae and P. canestrinii specimens, an infestation rate twice as high as for non-gobioid fishes in the lake. A possible explanation for this difference is the bottom-dwelling life style of both gobies. The glochidia of anadontin mussels are unable to swim actively and sink to the ground after they are released (Lefevre and Curtis, 1910; Paling, 1968; Dudgeon and Morton, 1984). Lake Trasimeno, however, is shallow (mean depth 4.7 m), and most fishes probably more or less often come close to the bottom or in direct contact with it. The tench T. tinca, for example, lives close to the bottom where it searches for food, even by digging in the sediment (Banarescu, 1999). Nonetheless, only about one quarter of the tench specimens were infested (Giusti et al., 1975).

Another potential explanation for the high infestation rate of the two gobies compared to the other fishes in the lake is a different reaction of their immune systems. Naïve specimens are most at risk if infestation (Rogers-Lowery and Dimock, 2006; Modesto et al., 2018). After a first infestation the immune system of perennial species learns to avoid or at least reduce infestation with glochidia. Accordingly, the young-of-the-year specimens of a host species generally carry a relatively higher glochidia burden than older conspecifics (Dodd et al., 2005; Barnhart et al., 2008; Donrovich et al., 2017). Both sand goby species are annual and therefore all specimens are naïve in this respect.

Beyond the degree of infestation, we also investigated the pattern of glochidia attachment on the fish body. This pattern on K. panizzae and P. canestrinii was generally similar to those of the fishes investigated by Giusti et al. (1975), with most glochidia attached to the fins and the head. Nearly no glochidia were attached on the trunk or tail. This also agrees with other studies, which found preferable attachment on the fins and head (e.g., McMahon and Bogan, 2001; Šlapansky et al., 2016; Mineeva and Semenov, 2021a, b). Giusti et al. (1975) concluded that the negligible attachment to the trunk and tail was linked to the scale cover of these body parts.

A deviation from the observations of Giusti et al. (1975) was the infestation of the caudal fin of Canestrini's goby. Those authors documented a relatively low rate on this fin for the lake fishes. The rate was also similarly low on the caudal fin of K. panizzae, but it was twice as high on the caudal fin of P. canestrinii and similar to the infestation rate of the paired fins of this species. Both species occur sympatrically at the sampling station. The infestation rate of the caudal fin is about 4.5 times larger in P. canestrinii than K. panizzae. Sampling was conducted at the beginning of the spawning season, when males probably already started to occupy territories. Possibly differences in microhabitat use of the males of the two species are responsible for the distinct difference in glochidia attachment on the caudal fins of both species.

Šlapansky et al. (2016) also reported a higher infestation of the caudal fin in juvenile Neogobius melanostomus (Pallas 1814) and Proterorhinus semilunaris (Heckel 1837) but unfortunately most other studies fail to provide a detailed pattern of glochidia attachment (Mierzejewska et al., 2014; Tremblay et al., 2016; Mineeva and Mineev, 2020). Comparing the various studies of gobioid infestation leaves an ambivalent picture. Some studies report minor infestation rates, demonstrating that glochidia are rare gobioid parasites (e.g., Tyutin et al., 2013; Kvach et al., 2017, 2018; Zhokhov et al., 2017; Mineeva and Mineev, 2020; Mineeva and Semenov, 2021a). Others, however, recorded low rates in some gobiid species but a high value in a sympatric goby (e.g., Mierzejewska et al., 2014; Itoh et al., 2016). Again, others found high glochidia burdens (e.g., Antal et al., 2015; Šlapansky et al., 2016). If repeated infection decreases the risk of further infestation by boosting the immune response, this could explain the divergent infestation rates of perennial gobiid fishes. For example, a high glochidia load was reported by Antal et al. (2015) and Šlapansky et al. (2016); the former authors investigated an annual species, the latter young-of the-year of perennial species: both were naïve fishes and therefore probably more prone to infestation (Rogers-Lowery and Dimock, 2006; Modesto et al., 2018).

Statistical analysis did not support sexual dimorphism in the susceptibility of K. panizzae and P. canestrinii. Nevertheless, a trend for sexual bias of certain body regions is apparent in both species. Overall, sexual dimorphism in glochidia infestation is apparently rare or not investigated. Anodonta anatina is a generalist accepting a wide array of fish hosts and does not prefer a particular sex or body region (Nagel, 1985; Barnhart et al., 2008; Modesto et al., 2018). We therefore assume that the sexual bias of attached glochidia in the investigated gobies relate to the behavior of these fishes during breeding season, with males being more sedentary (guarding nests and fanning) and females more mobile in search of suitable mates.

The prevalence (number of fish with glochidia/total number of fish sampled) but not the mean abundance (glochidia per individual) in A. anatina in Lake Trasimeno was higher in K. panizzae and P. canestrinii than for other investigated fish species here (> 45% vs. < 32%). The mean abundance is relatively low in all examined species including the two gobies and was 1.6–2.2 for all investigated species except for P. fluviatilis (Giusti et al., 1975; this study). Surprisingly, P. fluviatilis, an open-water species, carried most glochidia (5.2) rather than the inherently bottom-dwelling gobies (Tab. 3).

Because fishes we sampled in the wild were preserved immediately, we do not know if the larval glochidia successfully metamorphosed into juvenile mussels. It is therefore unclear if K. panizzae and P. canestrinii serve as primary hosts (high proportion of glochidia metamorphoses into juveniles) or as marginal hosts (low metamorphosis rates) and how they affect the recruitment of A. anatina. As primary hosts they could enhance the recruitment of this native mussel. In contrast, however, they could also limit the recruitment as a sink for glochidia, i.e., if most glochidia that encyst fail to metamorphose to juveniles. The latter scenario has been suggested for a gobiid introduced into the Great Lakes (USA) (Barnhart and Baird, 2000; Tremblay et al., 2016) and is supported by a laboratory infestation in which infested gobies lost more than 98% of glochidia within two weeks (Taeubert et al., 2012). Finally, Moore and Clearwater (2021) found that non-native fish species were only marginal hosts and a sink for native freshwater mussels, which could also be the case for juvenile gobiids with a high prevalence of glochidia (Šlapansky et al., 2016).

The main advantage of a parasitic stage is thought to be the spreading of the mussel by host fishes (Kat, 1984; Haag and Warren, 1997). Most benthic gobioid species are not good swimmers and do not traverse large distances. This makes any substantial transport by the two gobies low. Nevertheless, for relative sedentary organisms such as mussels, even small-scale movements of fish hosts could aid dispersal. Further investigation is needed to test whether K. panizzae and P. canestrinii serve as primary hosts or as a sink for glochidia of the freshwater mussel A. anatina in Lake Trasimeno. This may become increasing important because the Ebro+Italian clade of A. anatina (Froufe et al., 2014, 2017) is locally restricted and apparently declining (Lopes-Lima et al., 2017).

Freshwater mussels are of great ecological importance. They filter and process suspended particles thus clearing the water and also mix sediments (Modesto et al., 2018). Many populations are diminishing because of water pollution, habitat destruction and the decline of host species (Douda et al., 2012; Zieritz and Aldridge, 2011; Lopes-Lima et al., 2017). World-wide not only populations of freshwater mussels but also populations of many freshwater fishes, hosts of the parasitic stage of the mussels, are declining (Modesto et al.., 2018). The loss of host fish availability can have severe effects on freshwater mussel dispersion and thus on the status of their populations (Schwalb et al., 2011; Douda et al., 2012; Froufe et al., 2014). Especially anadontin mussels which are generalists for fish hosts could benefit from exotic, introduced fish species where natural fish populations are diminishing. Recently, it has been demonstrated that glochidia of freshwater mussels also attach to introduced gobioid species (Ondračková et al., 2005; 2009; Antal et al., 2015; Šlapansky et al., 2016; Tremblay et al., 2016). With their benthic life-style gobioids occur close to the mussels and also come directly in contact with glochidia on the bottom of aquatic habitats. These introduced gobioids may have severe effects on freshwater mussel populations in two ways. They can be beneficial as new hosts but may also act as a sink if the attached glochidia cannot develop to young mussels (Šlapansky et al., 2016; Tremblay et al., 2016). The understanding of the fish-mussel relationship, including non-native fish species which get increasingly important in many aquatic habitats, is essential for conservation management of freshwater mussels (Lopes-Lima et al., 2017; Modesto et al., 2018).

5 Conclusions

Two gobiid species, K. panizzae and P. canestrinii, translocated in Lake Trasimeno (Italy), are hosts for the parasitic stage of anodontin freshwater mussels. Although two mussels, the native A. anatina and the east Asian S. woodiana, are sympatric at the sampling locality, both fish species were infested only with glochidia of A. anatina. Host identification and the documentation of their benefits or threats for the interaction of the mussels with their hosts is an important baseline for conservation of freshwater mussels. But the co-existence of mussels with non-native fish species is only poorly understood, including the compatibility of these two groups. Extended work is required to identify (i) if the glochidia of two more native anadontins (A. cygnaea and A. exulcerata) also attach on these fishes, (ii) if the absence of glochidia of the introduced S. woodiana is a seasonal bias and (iii) in terms of conservation management, if the glochidia develop to juvenile mussels or if the two sand gobies are a possible sink for the freshwater mussels of Lake Trasimeno.

Author's contribution

HA conceived the study and wrote the manuscript. AC and ML collected the fishes, conducted statistical analysis and contributed to the writing of the manuscript. LK genetically identified the mussel parasites and contributed to the writing of the manuscript. TL contributed to the data sampling. MD identified the adult mussel shells and contributed to the manuscript. All authors read and improved the final version of the manuscript.

Acknowledgements

We thank Christoph Hörweg for his support with the photographs of glochidia-infested fishes and Benoit Lebreton for language editing of the French abstract. We also thank Michael Stachowitsch and two anonymous reviewers for valuable comments and suggestions.

References

  • Ahnelt H, Konecny R, Gabriel A, Bauer A, Pompei L, Lorenzoni M, Sattmann H. 2018. First report of the parasitic copepod Lernaea cyprinacea (Copepoda: Lerneidae) on gobioid fishes (Teleostei: Gobionellidae) in southern Europe. Knowl Mang Aquat Ecosyst 419: 34. [CrossRef] [EDP Sciences] [Google Scholar]
  • Antal L, Székely C, Molnár K. 2015. Parasitic infections of two invasive fish species, the Caucasian dwarf goby and the Amur sleeper in Hungary. Acta Vet Hung 63: 472–484. [CrossRef] [PubMed] [Google Scholar]
  • Banarescu P. 1999. The Freshwater Fishes of Europe. Vol. 5/I. Cyprinidae 2. Part I: Rhodeus to Capoeta. Wiebelsheim: Aula Verlag, 426 p. [Google Scholar]
  • Barnhart MC, Baird MS. 2000. Fish hosts and culture of mussel species of special concern: Annual report for 1999. Rep Missouri Dep Conserv, Columbia, Missouri, 21p. [Google Scholar]
  • Barnhart MC, Haag WR, Roston WN. 2008. Adaptations to host infection and larval parasitism in Unionoida. J N Am Benthol Soc 27: 370–394. [CrossRef] [Google Scholar]
  • Blažek R, Gelnar M. 2006. Temporal and spatial distribution of glochidial larval stages of European unionid mussels (Mollusca: Unionidae) on host fishes. Folia Parasit 53: 98–106. [CrossRef] [Google Scholar]
  • Borroni I. 1976. Involontaria introduzione nel Lago Trasimeno (Umbria) di un gobide di acqua salmastra (Knipowitschia panizzae) e seguito di pratiche ittiogeniche. Mem Ital Idrobiol 33: 297–304. [Google Scholar]
  • Carosi A, Ghetti L, Padula R, Lorenzoni M. 2019. Potential effects of global climate change on fisheries in the Trasimeno Lake (Italy), with special reference to the goldfish Carassius auratus invasion and the endemic southern pike Esox cisalpinus decline. Fish Manag Ecol 26: 500–511. [CrossRef] [Google Scholar]
  • Dartnall HJG, Walkey M. 1979. The distribution or glochidia of the Swan mussel, Anodonta cygnea (Mollusca) on the Three-spined stickleback Gasterosteus aculeatus (Pisces). J Zool, Lond 189: 31–37. [CrossRef] [Google Scholar]
  • Dodd BJ, Barnhart MC, Rogers-Lowery CL, Fobian TB, Dimock RV. 2005. Cross-resistance of largemouth bass to glochidia of unionid mussels. J Parasitol 91: 1064–1072. [CrossRef] [PubMed] [Google Scholar]
  • Donrovich SW, Douda K, Plechingerová V, Rylková K, Horky P, Slavík O, Liu H-Z, Reichard M, Lopes-Lima N, Sousa R, 2017. Invasive Chinese Pond mussel Sinanodonta woodiana threatens native mussel reproduction by inducing cross-resistance of host fish. Aquatic Conserv: Mar Freshw Ecosyst 27: 1325–1333. [CrossRef] [Google Scholar]
  • Douda K, Horky P, Bíly M. 2012. Host limitation of the thick-shelled river mussel: identifying the threats to declining affiliate species. Animal Conserv 15: 536–544. [CrossRef] [Google Scholar]
  • Duda M, Schindelar J, Macek O, Eschner A, Kruckenhauser L. 2017. First record of Trochlus clandestinus (Hartmann, 1821) in Austria (Gastropoda: Eupulmonata: Hygromiidae). Malacol Bohemoslov 16: 37–43. [CrossRef] [Google Scholar]
  • Dudgeon D, Morton B. 1984. Site selection and attachment duration of Anodonta woodiana (Bivalvia: Unionacea) glochidia on fish hosts. J Zool, Lond 204: 355–362. [CrossRef] [Google Scholar]
  • Emde S, Kochmann J, Kuhn T, Plath M, Klimpel S. 2014. Getting what is served? Feeding ecology influencing parasite-host interactions in invasive Round goby Neogobius melanostomus. PLoS ONE 9: e109971. [Google Scholar]
  • Francová K, Ondračková M, Polačik M, Jurajda P. 2011. Parasite fauna of native and non-native populations of Neogobius melanostomus (Pallas, 1814) (Gobiidae) in the longitudinal profile of the Danube River. J Appl Ichthyol 27: 879–886. [CrossRef] [Google Scholar]
  • Freyhof J. 1998. First record of Pomatoschistus canestrinii (Ninni, 1883) in Lake Trasimeno. Riv Idrobiol 37: 107–108. [Google Scholar]
  • Froufe E, Lopes-Lima M, Riccardi N, Zaccara S., Vanetti I, Lajtner J, Teixeira A, Varandas S, Prié V, Zieritz A, Sousa R, Bogan AE. 2017. Lifting the curtain on the freshwater mussel diversity of the Italian Peninsula and Croatian Adriatic coast. Biodivers Conserv 26: 3255–3274. [CrossRef] [Google Scholar]
  • Froufe E, Sobral C, Teixeira A, Souse R, Varandas S, Aldridge DC, Lopes-Lima M. 2014. Genetic diversity of the pan-European freshwater mussel Anodonta anatina (Bivalvia: Unionoida) based on CO1: new phylogenetic insights and implications for conservation. Aquatic Conserv: Mar Freshw Ecosyst 24: 561574. [CrossRef] [Google Scholar]
  • Giardino C, Bresciani M, Villa P, Martinelli A. 2010. Application of remote sensing in water resource management: the case study of Lake Trasimeno, Italy. Water Res Manag 24: 3885–3899. [CrossRef] [Google Scholar]
  • Giusti F, Castagnolo L, Moretti Farina L, Renzoni A. 1975. The reproductive cycle and the glochidium of Anodonta cygnea L. from Lago Trasimeno (Central Italy). Monit Zool Ital 9: 99–118. [Google Scholar]
  • Grabowska J, Kvach Y, Rewicz T, Pupins M, Kutsokon I, Dykyy I, Antal L, Zieba G, Rakauskas V, Trichkova T, Čeirāns, Grabowski M. 2020. First insight into the molecular population. Structure and origins of the invasive Chinese sleeper, Perccottus glenii, in Europe. NeoBiota 57: 87–107. [CrossRef] [Google Scholar]
  • Graf DL. 1997. Sympatric speciation of freshwater mussels (Bivalvia: Unionoidea): a model. Amer Malacol Bull 14: 35–40. [Google Scholar]
  • Haag WR, Warren ML. 1997. Host fishes and reproductive biology of 6 freshwater mussel species from the Mobile Basin, USA. J N Am Benthol Soc 16: 576–585. [CrossRef] [Google Scholar]
  • Haag WR, Warren ML. 2003. Host fishes and infection strategies of freshwater mussels in large Mobile Basin streams, USA. J N Am Benthol Soc 22: 78–91. [CrossRef] [Google Scholar]
  • Hanrahan NJ. 2019. Field and laboratory investigations of Echyridella menziesii (Unionida: Hyriidae) interactions with host fish. Masterthesis, University of Waikato, New Zealand. [Google Scholar]
  • Horky P, Douda K, Maciak M, Závorka L, Slavík O. 2014. Parasite-induced alterations of host behaviour in a riverine fish: the effects of glochidia on host dispersal. Freshw Biol 59: 1452–1461. [CrossRef] [Google Scholar]
  • Ieshko EP, Geist J, Murzina SA, Veselov AE, Lebedeva DI, Ziuganov VV. 2016. The characteristics of the infection of juvenile Atlantic salmon with glochidia of the freshwater pearl mussel in rivers of Northwest Russia. Know Manag Aquat Ecosyt 417: 6. [CrossRef] [EDP Sciences] [Google Scholar]
  • Itoh T. 2019. Host fish species for glochidia of the freshwater unionid mussel Sinanodonta sp. from Lake Biwako in autumn. Venus 77: 27–35. [Google Scholar]
  • Itoh T, Saitoh Y, Satoh Y, Ito K. 2016a. A new record of host fish Gymnogobius sp. for glochidia of Pronodularia japanensis, and the availability of host species for the mussel at three paddy field ditches in the Kanto area of central Japan. Jap J Limnol 77: 281–291. [CrossRef] [Google Scholar]
  • Itoh T, Uesugi S, Kakino W. 2016b. Host fish species for glochidia of the freshwater unionid mussel Cristaria plicata in tanks. Venus 74: 79–88. [Google Scholar]
  • Jansen W, Bauer G, Zahner-Meike E. 2001. Glochidial mortality in freshwater mussels. In Bauer G, Wächtler K, eds. Ecology and Evolution of the Freshwater Mussels Unionoida. Ecological Studies (Analysis and Synthesis), 145. Springer, Berlin, Heidelberg, 185–211. [Google Scholar]
  • Kat PW. 1984. Parasitism and the Unionacea (Bivalvia). Biol Rev 59: 189–207. [CrossRef] [Google Scholar]
  • Kirjušina M, Lazdāne M, Zolos M. 2014. Parasitofauna of Perccottus glenii Dybowski, 1877 (Osteichthyes, Odontobutidae) in water bodies of the southern part of Latgale (Latvia). Acta Biol Univ Daugavp 14: 137–143. [Google Scholar]
  • Klunzinger MW, Beatty SJ, Morgan DL, Thomson GJ, Lymbery AJ. 2012. Glochidia ecology in wild fish populations and laboratory determination of competent host fishes for an endemic freshwater mussel of south-western Australia. Australia J Zool 60: 26–36. [CrossRef] [Google Scholar]
  • Koubkova B, Barus V. 2000. Metazoan parasites of the recently established tubenose goby (Proterorhinus marmoratus: Gobiidae) population from the South Moravian reservoir, Czech Republic. Helminthologia 37: 89–95. [Google Scholar]
  • Kvach, Y, Kutsokon Y, Janác M, Dykyy I, Dzyziuk N, Dudliv I, Nazaruk K. 2022. Parasites of the invasive sleeper Perccottus glenii (Actinopterygii: Odontobutidae) in the region of the first introduction of the Carpathian population. Ocean Hydrobiol Studies 51: 1–9 [CrossRef] [Google Scholar]
  • Kvach Y, Mierzejewska K, Dziekońska-Rynko J. 2009. The parasites of two gobiids (Apollonia fluviatilis and Babka gymnotrachelus) in native range of southern Ukraine. XIV Conference of the Ukraine Scientific Society of Parasitologists, Uzghorod, 21–24 September 2009: 146. [Google Scholar]
  • Kvach Y, Ondračková M. 2020. Checklist of parasites of Ponto-Caspian gobies (Actinopterygii: Gobiidae) in their native and non-native ranges. J Appl Ichthyol 36: 472–500. [CrossRef] [Google Scholar]
  • Kvach Y, Ondračková M, Janač M, Jurajada P. 2017. The parasite community of round goby Neogobius melanostomus (Pallas, 1814) (Actinopterygii: Gobiidae) newly introduced into the upper Elbe. Knowl Manag Aquat Ecosyst 418: 19. [CrossRef] [EDP Sciences] [Google Scholar]
  • Kvach Y, Ondračková M, Trichkova T, Crobiniak O, Zamorov V, Jurajada P. 2018. Parasitization of monkey goby, Neogobius fluviatilis (Pallas, 1814) (Actinopterygii: Gobiidae), at localities with different salinity levels. Oceanol Hydrobiol St 47: 376–383. [CrossRef] [Google Scholar]
  • Lefevre G, Curtis WC. 1910. Studies on the reproduction and artificial propagation of fresh-water mussels. Bull Bur Fish 30: 105–201. [Google Scholar]
  • Lopes-Lima M, Sousa R, Geist J, Aldrige DC, Araujo R, Bergengren J, Bespalaya Y, Bódis E, Burlakova L, Van Damme D, Douda K, et al. 2017. Conservation status of freshwater mussels in Europe: state of the art and future challenges. Biol Rev 92: 572–607. [CrossRef] [Google Scholar]
  • Lorenzoni M, Mearelli M, Ghetti L. 2006. Native and exotic fish species in the Tiber River watershed (Umbria − Italy) and their relationship to the longitudinal gradient. Bull Fr Pêche Piscic 382: 19–44. [CrossRef] [EDP Sciences] [Google Scholar]
  • Lorenzoni M, Ghetti L, Pedicillo G, Carosi A. 2010. Analysis of the biological features of the goldfish Carassius auratus auratus (Linnaeus, 1758) in Lake Trasimeno (Umbria, Italy) with a view to drawing up plans for population control. Folia Zool 58: 56–70. [Google Scholar]
  • Lorenzoni M, Giannetto D, Carosi A, Dolciami R, Ghetti L, Pompei L. 2015. Age, growth and body condition of big-scale sand smelt Atherina boyeri Risso, 1810 inhabiting a freshwater environment: Lake Trasimeno (Italy). Knowl Mang Aquat Ecosyst 416, 09. [CrossRef] [EDP Sciences] [Google Scholar]
  • Ludovisi A, Gaino E. 2010. Meteorological and water quality changes in Lake Trasimeno (Umbria, Italy) during the last fifty years. J Limnol 69: 174–188. [CrossRef] [Google Scholar]
  • Maganelli G, Bodon M, Favilli L, Castagnolo L, Giusti F. 1998. Checklist delle species della fauna d'Italia, molluschi terrestri e d'acqua dolce. Errata ed addenda, 1. Boll Malacol, Roma 33: 151–156. [Google Scholar]
  • Martel AL, Lauzon-Guay J-S. 2005. Distribution and density of glochidia of the freshwater mussel Anodonta kennerlyi on fish hosts in lakes of the temperate rain forest of Vancouver Island. Can J Zool 83: 419–431. [CrossRef] [Google Scholar]
  • McMahon RF, Bogan AE. 2001. Mollusca: Bivalvia. In Thorp JH, Covich AP eds. Ecology and classification of North American freshwater invertebrates. 2nd ed. Academic Press. [Google Scholar]
  • Mearelli M, Lorenzoni M, Mantilacci L. 1990. Il Lago Trasimeno. Riv Idribiol 29: 353–389. [Google Scholar]
  • Mierzejewska K, Kvach Y, Stánczak K, Grabowska J, Wozniak M, Dziekońska-Rynko J, Ovcharenko M. 2014. Parasites of non-native gobies in the Włocławek Reservoir on the lower Vistula River, first comprehensive study in Poland. Knowl Mang Aquat Ecosyst 414: 01. [Google Scholar]
  • Miller PJ. 2004. The Freshwater Fishes of Europe. Vol. 8/II. Gobiidae 2. Wiebelsheim: Aula Verlag, 477 p. [Google Scholar]
  • Mineeva OV, Mineev AK. 2020. The first data on parasites of the Monkey goby Neogobius fluviatilis (Perciformes, Gobiidae) in the Saratov Reservoir. Russian J Biol Inv 11: 341–347. [CrossRef] [Google Scholar]
  • Mineeva OV, Semenov DY. 2021a. The parasite fauna of the round goby Neogobius melanostomus (Perciformes, Gobiidae) in the Kuybyshev reservoir (Middle Volga). Russian J Biol Inv 12: 83–93. [CrossRef] [Google Scholar]
  • Mineeva OV, Semenov DY. 2021b. First data on parasites of Neogobius iljini (Perciformes, Gobiidae) of the middle Volga. Russian J Biol Inv 12: 362–372. [CrossRef] [Google Scholar]
  • Modesto V, Ilarri M, Souza AT, Lopes-Lima M, Douda K, Clavero M, Sousa R. 2018. Fish and mussels: importance of fish for freshwater mussel conservation. Fish Fisheries 19: 244–259. [CrossRef] [Google Scholar]
  • Molnár K. 2006. Some remarks on parasitic infections of the invasive Neogobius spp. (Pisces) in the Hungarian reaches of the Danube River, with a description of Goussia szekelyi sp. n. (Apicomplexa: Eimeriidae). J Appl Ichthyol 22: 395–400 [CrossRef] [Google Scholar]
  • Moore TP, Clearwater SJ. 2021. Non-native fish as glochidial sinks: elucidating disruption pathways for Echyridella menziesii recruitment. Hydrobiologia 848: 3191–3207. [CrossRef] [Google Scholar]
  • Muzzal PM, Pebles CR, Thomas MV. 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. J Helminthol Soc Wash 62: 226–228. [Google Scholar]
  • Nagel K-O. 1985. Glochidien und Fortpflanzungsbiologie von Najaden des Rheins (Bivalvia − Unionidae − Anadontinae). Mainz Naturw Arch 5: 163–175. [Google Scholar]
  • Nagel K-O, Castagnolo L. 1991. Fish hosts for the glochidium of Unio mancus. Riv Idrobiol 30: 2–3. [Google Scholar]
  • Ondračkova M, Dávidová M, Blažek R, Gelnar M, Jurajda P. 2009. The interaction between an introduced fish host and local parasite fauna: Neogobius kessleri in the middle Danube River. Parasitol Res 105: 201–208. [CrossRef] [PubMed] [Google Scholar]
  • Ondračkova M, Dávidová M, Pečniková M, Blažek R, Gelnar M, Valová Z, Černy J, Jurajda P. 2005. Metazoan parasites of Neogobius fishes in the Slovak section of the River Danube. J Appl Ichthyol 21: 345–349. [CrossRef] [Google Scholar]
  • Ondračkova M, Janáč M, Borcherding J, Grabowska J, Bartáková V, Jurajda P. 2021. Non-native gobies share predominantly immature parasites with local fish hosts. J Vert Biol 70: 21050. [Google Scholar]
  • Ondračkova M, Trichkova T, Jurajda P. 2006. Present and historical occurrence of metazoan parasites in Neogobius kessleri (Pisces: Gobiidae) in the Bulgarinan section of the Danube River. Acta Zool Bulgar 58: 401–408. [Google Scholar]
  • Ondračkova M, Valovà Z, Hudocvá I, Michálková V, Šimková A, Borcherding J, Jurajda P. 2015. Temporal effects on host-parasite associations in four naturalized goby species living in sympatry. Hydrobiologia 746: 233–243. [CrossRef] [Google Scholar]
  • Paling JE. 1968. A method of estimating the relative volumes of water flowing over the different gills of a freshwater fish. J Exp Biol 48: 533–544. [CrossRef] [PubMed] [Google Scholar]
  • Panha S. 1992. Infection experiment of the glochidium of a freshwater pearl mussel, Hyriopsis (Limnoscapha) myersinana (Lea, 1856). Venus 51: 303–314. [Google Scholar]
  • Patzner RA. 2004. Bivalves and their host fishes. Österr Fischerei 57: 278–281 [in German with English summary]. [Google Scholar]
  • Reuling FH. 1919. Acquired immunity to an animal parasite. J Infect Dis 24: 337–346. [CrossRef] [Google Scholar]
  • Reshentikov AN. 2013. Spatio-temporal dynamics of the expansion of rotan Perccottus glenii from West-Ukrainian centre of distribution and consequences for European ecosystems. Aquatic Inv 8: 193–206. [CrossRef] [Google Scholar]
  • Riccardi N, Froufe E, Bogan AE, Zieritz A, Teixeira A, Vanetti I, Varandas S, Zaccara S, Nagel K-O., Lopes-Lima M. 2020. Phylogeny of European Anodontini (Bivalvia: Unionidae) with a redescription of Anodonta exulcerata. Zool J Linn Soc 189: 745–761. [CrossRef] [Google Scholar]
  • Rogers-Lowery CL, Dimock RV. 2006. Encapsulation of attached ectoparasitic glochidia larvae of freshwater mussels by epithelial tissue on fins of naïve and resistant host fish. Biol Bull 210: 51–63. [CrossRef] [PubMed] [Google Scholar]
  • Rolbiecki L. 2006. Parasites of the round goby, Neogobius melanostomus (Pallas, 1811), an invasive species in the Polish fauna of the Vistula Lagoon ecosystem. Oceanologia 48: 545–561. [Google Scholar]
  • Schwalb AN, Cottenie K, Poos MS, Ackerman JD. 2011. Dispersal limitation of unionid mussels and implications for their conservation. Freshw Biol 56: 1509–1518. [Google Scholar]
  • Shimizu T, Nagasawa K. 2018. Four species of acanthocephalans parasitic in freshwater gobies Rhinogobius ssp. in western and central Japan, with a list of the known parasites of Rhinogobius ssp. of Japan (1935–2018). Bull Hirosh Univ Mus 10: 37–52. [Google Scholar]
  • Šlapansky L, Jurajda P, Janác M. 2016. Early life stages of exotic gobiids as new hosts for unionid glochidia. Freshw Biol 61: 979–990. [CrossRef] [Google Scholar]
  • Taeubert J-E., Gum B, Geist J. 2012. Host-specificity of the endangered thick-shelled river mussel (Unio crassus, Philipsson 1788) and implications for conservation. Aqu Cons Mar Freshw Ecosyst 22: 36–46. [CrossRef] [Google Scholar]
  • Thacker CE. 2009. Phylogeny of Gobioidei and placement within Acanthomorpha, with a new classification and investigation of diversification and character evolution. Copeia 2009: 93–104. [CrossRef] [Google Scholar]
  • Tremblay MEM, Morris TJ, Ackerman JD. 2016. Loss of reproductive output caused by an invasive species. R. Soc. Open Sci 3: 150481. [CrossRef] [Google Scholar]
  • Tyutin AV, Verbitsky VB, Verbitskaya TI, Medyantseva EN. 2013. Parasites of aquatic animals in the Upper Volga Basin. Russian J Biol Inv 4: 54–59. [Originally published in Ross Z Biol Inv 2012 (4): 96-105; in Russian]. [CrossRef] [Google Scholar]
  • Watters GT. 1994. An annotated bibliography of the reproduction and propagation of the Unionoidea (primarily of North America). Misc Contrib Ser Ohio Biol Surv Ohio State Univ. [Google Scholar]
  • Zieritz A, Aldridge DC. 2011. Sexual, habitat-constrained and parasite-induced dimorphism in the shell of a freshwater mussel (Anodonta anatina, Unionidae). J Morphol 272: 1365–1375. [CrossRef] [PubMed] [Google Scholar]
  • Zhokhov AE, Pugacheva MN, Molodozhnikova NM. 2017. Parasites of the invasive goby Proterorhinus semiluniaris (Pisces: Gobiidae) in Rybinsk Reservoir and checklist of their parasites of gobiids (Genus Proterorhinus) in Eurasia. Russian J Biol Inv 8: 18–33. Originally published in Ross Z Biol Inv 2016, 4: 24–40 [in Russian]. [CrossRef] [Google Scholar]

Cite this article as: Ahnelt H, Leister T, Kruckenhauser L, Duda M, Carosi A, Lorenzoni M. 2023. Site-specific attachment of Anodonta anatina (Bivalvia: Unionidae) glochidia on two new fish hosts translocated in Lake Trasimeno (Italy). Knowl. Manag. Aquat. Ecosyst., 424, 9.

All Tables

Table 1

Knipowitschia panizzae and Pomatoschistus canestrinii from Lake Trasimeno; number (N) of specimens with glochidia of Anodonta anatina attached to different parts of the body in total and by sex. A = anal fin, C = caudal fin, D1, D2 = first and second dorsal fin, P = pectoral fins and V = pelvic fins (fused to pelvic disc).

In the text
Table 2

Knipowitschia panizzae and Pomatoschistus canestrinii from Lake Trasimeno; sampling dates from March − May 2022 with number of specimens in total and, in parentheses, females/males, of not infested and infested specimens.

In the text
Table 3

Fish species of Lake Trasimeno infested with glochidia of Anodonta anatina * (this study) and Anodonta sp.**. Ab = Atherina boyeri, Kp = Knipowitschia panizzae, Lg = Lepomis gibbosus, Pc = Pomatoschistus canestrinii, Pf = Perca fluviatilis, Tt = Tinca tinca.

In the text
Table 4

Percentage of glochidia attachment on the four most infested structures of Knipowitschia panizzae and Pomatoschistus canestrinii separated by species and, within species, by sex. C = caudal fin, P = pectoral fin and V = pelvic fin (sucking disc).

In the text
Table 5

Infestation (mean number) of Knipowitschia panizzae and Pomatoschistus canestrinii with glochidia of Anodonta anatina and water temperature of Lake Trasimeno during sampling period. *April 22: only one, not infested, specimen of K. panizzae was collected.

In the text
Table 6

Literature survey of gobioid fishes infested with glochidia of Unionidae (Bivalvia: Unionida). Gobioidei infested with glochidia: n = 33 (Graf (1997), who just mentioned “goby”, is not included in this number). The eight species listed by Modesto et al. (2018) are shaded in grey. Note, that for each species/country just one publication, as example, is listed.

In the text

All Figures

thumbnail Fig. 1

A: map of Italy showing location of Lake Trasimeno and location of sampling site (red dot). B: sampling site at Monte del Lago. Photo A. Carosi.
In the text
thumbnail Fig. 2

Glochidia of Anodonta anatina (black arrows) attached to hosts Pomatoschistus canestrinii (NHMW-MO-113655) (A, B) and Knipowitschia panizzae (NHMW-MO-113654) (C, D). Parasites attached to A: the pectoral and the pelvic fins (united to pelvic disc); B: same specimen, encysted glochidium, right pectoral fin; C: base of pectoral disc; D: same specimen, pectoral disc enlarged. Scale of A, C = 5 mm; scale of B, D = 1 mm. Photos C. Hörweg, H. Ahnelt.
In the text

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