Spinitectus inermis (Nematoda: Cystidicolidae) in the European Eel, Anguilla anguilla (Pisces, Teleostei) from the Mesima River (Southern Calabria, Italy)

Abstract

The nematode Spinitectus inermis (Zeder, 1800), a specific gastrointestinal parasite of Anguilla anguilla, has been recorded for the first time in the Italian Peninsula. The study was conducted in the Mesima River, located in the southwestern part of the Calabria region (southern Italy). Over a five-month period, 162 specimens of European eel were sampled, revealing an overall prevalence of 47.53%, a mean intensity of 9.51 (±13.88), and a mean abundance of 4.55 (±10.69). The nematode was present throughout the five months analyzed, with prevalence rates ranging from 32.0% to 57.14%. The overall prevalence in the Mesima River was higher than in most previous studies, and the mean abundance of infection was also higher. The highest prevalence of infection was observed in September (56.7%), October (57.14%), November (48.57%), and December (40.54%), with the lowest in March (32.0%). In conclusion, Spinitectus inermis appears to be well established in the eel population of the Mesima River, exhibiting high prevalence and intensity year-round despite ecological variations, though its intermediate hosts remain unknown.

1. Introduction

The European eel (Anguilla anguilla Linnaeus 1758) is naturally widespread throughout western Europe in rivers, lakes, and coastal lagoons. Its range has been extended to landlocked inland waters through stocking and farming [1]. Due to its commercial importance, its parasite fauna is well known and has been extensively studied throughout its distribution range [2]. According to [3], a total of 161 parasite species have been recorded in the European eel from 30 European and North African countries. Among them is the nematode Spinitectus inermis (Zeder, 1800), a specific gastrointestinal parasite of A. anguilla [4], which is widely distributed across Europe (North, Baltic, and Mediterranean Sea basins) but occurs only locally [5], with very few known localities [1]. It was later reported by [4] in the Czech Republic, [2] in Latvia, and [6] on the island of Sardinia. The compilation of [1] available data concluded that S. inermis should be considered a rare species, with a restricted and low frequency of occurrence, exhibiting diffusive rarity. No data exist on the presence of this nematode in the Italian Peninsula; however, the present study’s finding of S. inermis in an Italian river allows us to examine its distribution in an eel population.

The Mesima River is located in the southwestern part of the Calabria region (southern Italy) and flows into the Tyrrhenian Sea [7]. The river exhibits a torrential regime, with significant floods during the winter months and low flows in the summer. This river serves as a natural habitat for A. anguilla (Linnaeus, 1758) [8].

2. Materials and Methods

A total of 162 specimens of European eels were sampled from the Mesima River (38°29′47.87″ N/15°58′18.27″ E) between September and December 2016, using the method of electrofishing (SCUBLA 1300 W backpack electro-fisher, Remanzacco, Italy) along a 2 km transect. After capture, the eels were transported alive to the Parasitology Laboratory of the Department of Ecology, Biology, and Earth Sciences at the University of Calabria (Italy). The eels were euthanized using eugenol [9], and, for each fish, the total body length (cm) and weight (g) were recorded [10]. The gastrointestinal tracts (stomach and intestine) of all individuals were removed and examined for the presence of Spinitectus inermis under a stereomicroscope [11]. Recovered nematodes were counted, washed in physiological saline, fixed in AFA (acetic acid–formalin–alcohol), and preserved in 70% ethanol. For light microscopic examination, each worm was mounted on semi-permanent slides with Aman’s lactophenol. The identification of S. inermis was carried out according to [12,13,14,15]. In addition, ten adult males were measured for large spicule, small spicule, and total body length, with results presented in micrometers and the median and range calculated for all measurements. Parasitological parameters (prevalence P%, mean intensity MI, and mean abundance MA) were calculated following the definitions of [16]. The results were analyzed using the Chi-Square test to determine the significance of observed associations. The relationships between eel length and weight, and both the abundance and intensity of S. inermis infection, were compared using Spearman’s correlation coefficient (rs) in the statistical program Instat 3.0.

3. Results

The total length and weight of eels ranged from 20.0 to 64.5 cm (mean = 29.53 ± 5.20 cm) and 14.0 to 528.0 g (mean = 54.62 ± 57.74 g), respectively. The infected eels (n = 77) with the presence of S. inermis (Figure 1a–f) were slightly larger (mean length 29.98 ± 4.92 cm) than the uninfected ones (n = 85; mean length = 29.12 ± 5.44 cm). In males of S. inermis (n = 10), the total body length averaged 9926 μm (13,899–6233 μm), the large spicule length 1018 μm (1089–951 μm), and the small spicule length from 152 μm (164–145 μm). The mature eggs on the uterus of females have the characteristic thin gelatinous polar caps.

Infected eels weighed less (50.93 ± 28.30 g) than the uninfected ones (57.96 ± 75.11 g). There were no significant differences between the infected and uninfected eels related to weight (χ² = 0.9; p < 0.7; df = 1). The differences in both parameters (length/weight) were not statistically significant (Mann–Whitney U-test: U = 2868.5; U′ = 3683.5; p = 0.17 for length; U = 3139.5; U′ = 3405.5; p = 0.65 for weight). Spinitectus inermis showed a prevalence of 47.53% (77/162), mean intensity of 9.51 (±13.88) parasites per infected fish, and mean abundance of 4.55 (±10.69). The intensity of infection varied from 1 to 87 parasites per eel, and the total number of nematodes found was 733; all parasites were collected from the eels’ stomachs. No significant correlation between eel length or weight and the abundance of Spinitectus inermis (Rho = 0.08, p = 0.28 for length; Rho = 0.02, p = 0.78 for weight) was found. Similarly, no significant correlation between eel length or weight and the intensity of S. inermis infection (Rho = −0.07; p = 0.52 for length; Rho = −0.05; p = 0.65 for weight) was observed. The nematode was present in all five months analyzed, with prevalence ranging from 32.0% to 57.14%. The prevalence of infection was highest in September (56.7%), October (57.14%), November (48.57%), and December (40.54%) and lowest in March (32.0%). No significant differences were found between the months (χ² = 5.46; p < 0.24; df = 4). The mean intensity was highest in March (18.12), decreased to 6.06 in December, and increased again in November, October, and December, recording values of 8.35, 10.6, and 8.29, respectively. Our results show that in December, the total number of parasites recovered from the examined fish was low (n = 91), whereas in March (n = 147), September (n = 141), October (n = 212), and November (n = 142), there was an increase. The number of parasites varied significantly across the months (χ² = 25.07; p < 0.0001; df = 4). Additionally, the Spearman test showed no significant correlation between either eel weight or length and the abundance of parasites across the months, except for a significant correlation in October (Rho = −0.39; p = 0.01 for weight; Rho = 0.38; p = 0.02 for length).

4. Discussion

To our knowledge, this is the first report of the nematode Spinitectus inermis parasitizing Anguilla anguilla in the Italian Peninsula. The only previous report of this nematode from this host species occurred in the northwestern Sardinia island, Alghero [6]. The overall prevalence of Spinitectus inermis (47.53%) reported in this study is higher than most previous studies: 3.0% in the Czech Republic [17]; 3.3%, 6.1%, 10.9%, and 7.40% in Poland [18,19]; 1.8%, 4.2%, and 6.0% in England [20,21,22]; 6.6% and 23.1% in Germany [3,23]; and 16.1% in Portugal [24]. In Spain, prevalence rates ranged from 0.2% to 18.9% [25,26], and, in Latvia, 1.3% was reported by [2]. However, our findings are similar to the prevalence of 40.0% reported by [27] in some localities, though other studies in England showed lower prevalences (18.9–28.6%). Several factors may contribute to these variations in S. inermis prevalence, including the parasite’s life cycle, which is partly influenced by seasonal variations [14,28], changes in environmental condition, and the density of intermediate hosts involved in the nematode’s life cycle. The mean intensity of S. inermis in the Mesima River (9.51) is higher than previous reports in the literature: 3.0 in [19]; 2.3–3.4 in [18]; 3.0 in [21]; 4.0–6.5 in [23]; 3.7–7.7 in [29]; 1.0–8.0 in [3]; 5.5 in [24]; 1.0 in [25]; 3.79–7.30 in [26]; and 7.0 in [20]. The high intensities of S. inermis infection in eels could be associated with high infection rates in the intermediate host population, which are assumed to be aquatic insect larvae, as shown in other representatives of the genus [30].

Eggs of S. inermis have thin gelatinous polar caps [5], which seem to have an adhesive function. This could cause the aggregation of several eggs during oviposition, leading to their intake by a single intermediate host, although the infection intensities in the intermediate host are not well known. In the current study, the mean abundance of S. inermis infection across all samples was 29.53 worms, which was higher than previously reported studies that recorded average intensities ranging from 0.002 to 5.6. Regarding the prevalence of S. inermis over the five months of study, the highest peaks were observed in September, October, November, and December at 56.7%, 57.14%, 48.57%, and 40.54%, respectively, while the lowest was in March at 32.0%. The higher infection rates during these months could be attributed to environmental condition favorable to the parasite and for the intermediate hosts. Although no seasonal studies have been conducted specifically on S. inermis, its rarity of occurrence suggests that seasonal dynamics might partly influence its infrequent presence (reviewed in [28]). The decrease in prevalence observed during certain months is limited, but the environmental conditions in southern Italy differ significantly from those in Central Europe and England, except for [5] in Portugal, where most studies have been performed. The absence of S. inermis in the Italian peninsula prior to our report may be due to the localized occurrence of this parasite, as previously shown [1,5], combined with the limited number of studies conducted in the Italian peninsula.

5. Conclusions

In conclusion, Spinitectus inermis appears to be well established in the eel population of the Mesima River. This parasite showed high prevalence and intensity throughout the year, despite variations in ecological conditions, though the intermediate hosts driving its population remain unknown.