Diversity of digeneans parasitizing Mullus barbatus and Mullus surmuletus (Teleostean, Mullidae) off the coast of Algerian

The host species (Perciformes: Mullidae Rafinesque, 1815) is one of the oldest known and appreciated fish; it is particularly important in the Mediterranean because it is of great economic and commercial interest (Busalacchi et al., 2010; Mangano et al., 2017; Carbonara et al., 2018). The family Mullidae is one of the largest families, consisting of sixty-two species divided into six genera (Nelson, 2006), of which three genera (Mullus, Upeneus, Pseudopeneus) have been recorded in the Mediterranean Sea (Hureau, 1986; Golani, 1994). The genus Mullus Linnaeus, 1758 is represented by two species, Mullus barbatus Linnaeus, 1758 and Mullus surmuletus Linnaeus, 1758, with a subspecies Mullus barbatus ponticus Essipov, 1927 from the Black Sea (Hureau, 1986; Turan, 2006). They are easily recognized by the presence of a pair of long, mobile hyoid barbels on the chin (Randall, 1983; Kim, 2002; Nelson, 2006). Their diet is varied, feeding on crustaceans, polychaetes and mollusks, and small fish, fish eggs and echinoderms (Platell & Potter, 2001; Platell et al., 1998; Stergiou & Karpouzi, 2001; Derbal et al., 2010). On the Algerian coast, the red mullet M. barbatus and the striped mullet M. surmuletus are very abundant and very frequent in commercial catches (Dieuzeide et al., 1955; Djabali et al., 1993; Derbal & Kara, 2001). These species are gregarious, but they do not share the same biotopes (Lombarte et al., 2000) nor the same trophic niches (Labropoulou & Eleftheriou, 1997) because M. barbatus is a demersal species, generally frequenting the mud, sand or gravel bottoms of the continental shelf, whereas M. surmuletus is a demersal species on the rock and gravel bottoms, but sometimes also on the soft bottoms (Fischer et al., 1987).

Many researchers have been interested in the study of the parasitic biodiversity of the genus Mullus because it has a rich parasitic fauna, especially the parasitic Digenea (Gaglio et al., 2011; Carreras-Aubets et al., 2012; Derbel et al., 2012; Hassani et al., 2012; Debenedetti et al., 2013; Bottari et al., 2014; Cinar, 2014; Hassani et al., 2015; Barreiro et al., 2017; Antar et al., 2018; Bottari et al., 2020).Despite all this work, few researchers are interested in epidemiological study using parasitological indices with statistical tests in the Mediterranean area.

This work aims to know the biodiversity of the Digenea parasites of these fishes collected along the Algerian coast and consequently the realization of a complete inventory. In a second step, we will carry out a bioecological approach to the parasites, where we will be particularly interested in the general characteristics of the parasitism, the parasite-host relationships and the parasite-host-environment relation will also be approached because the parasite indices of these two hosts at the same time is not detailed. We also used statistical tests to understand the functioning of parasitism and to compare our data with those available in the Mediterranean.

Between February 2019 and October 2021, a total of 507 specimens of M. barbatus and 123 specimens of M. surmuletus were collected from fish landings at the fishing harbor in different regions off the Algerian coast that extends from western [Ain Témouchent (35°17′22″ N, 1°08′28″ W) and Ghazaouet (35°06′0″ N, 1°51′0″ W)], to central [Cherchell (36°36′31″ N, 2°11′50″ E), Bouharoune (36°37′24″ N, 2°39′17″ E), Algiers (36°45′8″ N, 3°°2′31″ E), La pirouz (36°47′26″ N, 3°14′59″ E), Cap Djinet (36°52′37″ N, 3°43′23″ E), Dellys (36°54′48″ N, 3°54′51″ E) and Béjaïa (36°45′00″ N, 5°04′00″ E)] and the east [El Kala (36°53′44″ N, 8°26′36″ W) and Annaba (36°54′27″ N, 7°45′26″ W)] (Fig. 1). Fishes were kept on ice and transferred immediately to the laboratory (LBEIG, USTHB) shortly after capture. In the laboratory, each specimen was identified with keys (Fischer et al., 1987), weighed (g), measured in full length (cm) and dissected the digestive tract of goatfish were placed in separate Petri dishes containing seawater and observed under a Zeiss microscope for the presence of digenean parasites. The latter were kept in 70 % ethyl, stained with boracic carmine, dehydrated through a graded ethanol series, cleared in clove oil and mounted in Canada balsam as a permanent mount. Drawings were made with an optical microscope equipped with a drawing tube (ZEISS Axioskop) in the laboratory of Parasitology of the Faculty of Biological Sciences of the USTHB (Algeria). Drawings were scanned and redrawn on a computer with Adobe Illustrator (CS5). Parasitological indices first processed the results obtained in this research. Processed the results obtained in this research (Prevalence and abundance) were calculated following Margolis et al. (1982). For the statistical study, the Shapiro-Wilk normality test, the Kruskal-Wallis test, the Wilcoxon test, independence and homogeneity tests based on the distribution Chi-square was used, and factorial correspondence analysis (FCA).

Fig. 1.

All applicable institutional, national and international guidelines for the care and use of animals were followed.

The Examination of the digestive tract of 630 teleost hosts of the Mullidae collected along the Algerian coast allowed us to identify 1553 parasitic Digenea divided into sex species, which are attached to 5 families: Hemiuridae Looss, 1899 (Lecithocladium excisum (Rudolphi, 1819) Lühe, 1901 (Fig. 2A)), Fellodistomidae Nicoll, 1909 (Proctoeces maculatus (Looss, 1901) Odhner, 1911 (Fig. 2B)), Deogenidae Nicoll, 1910 (Derogenes latus Janiszewska, 1953 (Fig. 2C)), Monorchiidae Odhner, 1911 (Proctotrema bacilliovatum Odhner, 1911 (Fig. 2D)), Opecoelidae Ozaki, 1925 (Opecoeloides furcatus (Bremser in Rudolphi, 1819) Odhner, 1928 (Fig. 2E); Poracanthium furcatum Dollfus, 1948 (Fig. 2F)).

Fig. 2.

Our study included a total of 630 individuals, among which 196 were parasitized (31.11 %), including 507 Mullus barbatus with 138 parasitized individuals (27.22 %) and 123 Mullus surmuletus with 58 parasitized individuals (47.15 %); the Chi-square test (χ²=18.355) allowed us to detect a highly significant difference (P < 0.001) between the prevalence of parasitism according to the host species, that is to say M. surmuletus is more parasitized than M. barbatus with a higher prevalence. To compare the abundance of the different parasites observed between the two fish species, we first checked the normality with the Shapiro-Wilk test, it turns out that P < 0.05 so the abundance values of the parasites do not follow a normal distribution, for that we used the Wilcoxon rond test to compare the different parasite species between the host species, this last one showed us that there is not a significant difference with P > 0.05.

The most diverse parasite fauna was observed in M. surmuletus with six species of parasites, contrary to M. barbatus, which hosts only five species from which P. maculatus is absent. The prevalence values of the parasites according to the host species show a highly significant difference (Table 1); the fauna of these species was dominated by O. furcatus (24.60 %), followed by P. furcatum (5.87 %) and L. excisum (4.29 %) then D. latus (2.22 %), while P. bacilliovatum and P. maculatus had the lowest prevalences (1.43 % and 1.27 % respectively); there is a highly significant difference between the observed prevalences, so the Chi-square test of homogeneity showed the absence of homogeneity between the different parasite species with P < 0.001. On the other hand, O. furcatus and P. bacilliovatum were more abundant than the other parasitic Digenea (A= 1.89; A= 0.23 repectively) in Mullidae species (Table 1).

The interpretation of the results in Table 2 shows that the distribution of parasitic Digenea is not the same in the two host species, we noticed that the prevalences and abundances of the latter are higher in M. surmuletus than in M. barbatus. We also deduced that the distribution of the different parasitic species with a prevalence > 10 % is always high for O. furcatus in both species of Mullidae, while P. furcatum has a higher prevalence in M. surmuletus (14.63 %) than in M. barbatus (3.75 %).

The analysis in Table 3 highlights the mean prevalence and abundance of weight and size of the two red mullet species for each parasitic Digenea, the size values show that the highest prevalences and abundances are observed for the species O. furcatus (P = 19.44 %; A = 1.33) followed by P. furcatum and L. excisum (P = 5.30 %; A = 0.09, P = 4.04 %; A= 0.09 respectively) whose size is ≤ 16.5 cm, however fish with a size > to 16.5 cm are dominated by O. furcatus (P = 33.33 %; A = 2.83) followed by P. furcatum and L. excisum (P = 6.84 %; A = 0.21, P = 4.70 %; A= 0.24 respectively). Moreover, the lowest prevalence and abundance were observed in D. latus, P. maculatus and P. bacilliovatum (Table 3); the Chi-square test for prevalence was highly significant (P < 0.001), which explains that small fish are more parasitized than large fish. The other values also indicate that the highest prevalences and abundances for each parasite species are observed for O. furcatus (P = 24.33 %; A = 1.69) followed by P. furcatum and L. excisum (P = 5.83 %; A = 0.13, P = 4.00 %; A= 0.09 respectively) whose weight is ≤ 100g, while the second class of fish whose weight is > to 100g are dominated by O. furcatus (P = 30.00 %; A = 5.83) followed by D. latus, P. bacilliovatum, L. excisum and P. furcatum (P = 13.33 %; A = 0.20, P = 10 %; A= 1.70, P = 10 %; A = 1.27, P = 6.67 %; A = 0.20 respectively), but the lowest prevalence and abundances are still reported for P. maculatus (Table 3). The Chi-square test shows a highly significant difference (P < 0.001), indicating that small fish are more contaminated than large fish over 100g.

The prevalence and abundance values of the different species of red mullet parasites according to the sampling sites are shown in Table 4. The results show that the species P. maculatus infests only the red mullet fish M. surmuletus in central Algeria with a high prevalence and abundance rate (P = 15.69 %; A = 0.92), while O. furcatus and P. furcatum are reported in both species of red mullet in the center and the east, contrary to the west where the latter two are not reported in M. barbatus. Furthermore, it is noted that the species L. excisum is absent in the west for both species of fish and the east for M. barbatus in contrast to D. latus, which presents a very high infestation rate in the western fish (P = 100 %; A = 0.13, P = 100 %; A = 1.00) for M. barbatus and M. surmuletus respectively. Table 4, shows that the western individuals of M. barbatus are infested only by D. latus. Comparison of the abundance of M. barbatus and M. surmuletus by region using the Kruskal-Wallis test revealed a non-significant difference with P > 0.05.

The relationship between the infestation parameters and the four seasons of the year are presented in Table 5. The results show that both O. furcatus and P. furcatum are present all the year round in both host species, with an infestation rate that is high for O. furcatus in summer for M. barbatus and M. surmuletus (P = 89.29 %; A = 3.83, P = 95.00 %; A = 5.52 respectively) and we also noticed that L. excisum is absent in summer for M. barbatus but in the second M. surmuletus it is present throughout the year with a high infestation rate in winter (P = 50.00 %; A = 2.73), furthermore D. latus species is absent in M. surmuletus in spring and summer but has a high infestation rate in autumn (P = 21.43 %; A = 0.13), while the prevalence and abundance values of P. bacilliovatum according to the seasons show that the latter is absent in winter in both host species, in addition it is an uncommon parasite as it is not abundant in M. barbatus (Table 5) and for P. maculatus we noted that this species is only reported in M. surmuletus during the four seasons with a high prevalence rate in summer (20 %), but it is very abundant in autumn and spring (A = 1.16, A = 2.51 respectively).

Comparison of the abundance of M. barbatus and M. surmuletus by season using the Kruskal-Wallis test revealed a non-significant difference with P > 0.05, so there is no seasonal difference.

Correspondence factor analysis (CFA) (Fig. 3) was applied to reveal the distribution of parasitic species found in the two red mullet species according to season. The contribution of the parasitic Digenea found in the two red mullet species to the total inertia is 65.82 % for axis 1 and 21.05 % for axis 2. The sum of these two rates is equal to 86.88 %. All the information is contained in the plane of axes 1 – 2. The participation of the seasons in the formation of axes 1 and 2 is as follows: for axis 1, it is autumn with 28.12 % and spring with 28.41 % that are most involved in the construction of axis 1, while for axis 2, it is spring with 47.03 % and summer with 44.46 % that are most involved in the development of axis 2. While the participation of the parasitic Digenea in the formation of the two axes is as follows: The species that intervene most in the formation of axis 1 has a rate equal to 60.89 %; it is L. excisum. It is followed by D. latus, which participates with 18.04 %, then P. bacilliovatum and P. furcatum with 7.65 % and 6.32 %, respectively. The other species participate at lower rates. On the other hand, P. furcatum is the species that contribute most to the elaboration of axis 2, with a percentage that equals 46.95 %. Followed by P. maculatus with a percentage equal to 23.66 %. In contrast, O. furcatus and P. bacilliovatum come in the third position with 14.67 % and 13.95 %, respectively. The other species occur at lower rates. The distribution of the parasites by season is as follows: each quadrant represents a season; winter is in the first quadrant, spring in the second quadrant, summer in the third quadrant and autumn in the fourth quadrant, which indicates that the parasites are found throughout the different seasons. The scatter plot shows that O. furcatus is represented throughout the year, so it is an omnipresent species. On the other hand, it shows that L. excisum is a species that predominates in autumn and winter, unlike P. furcatum and P. maculatus, which are predominant in summer. In particular, we note that spring is a season represented only by P. bacilliovatum and autumn by D. latus, that is to say, where the infestation is high.

Fig. 3.

Studies of the parasitic fauna of the Digenea parasites of the two species of red mullet M. barbatus and M. surmuletus with their bioecological analyses along the Algerian coast are rare and fragmentary.

Of the 1553 parasites collected, we found six species of Digenea parasites in M. surmuletus and five species in M. barbatus that belong to different families. Concerning M. surmuletus, our results are similar to those of Brahim Tazi et al. (2009). While in western Algeria, Haddad et al. (2013) and Hassani et al. (2015) reported the same species of Digenea parasite except for P. maculatus. In the Mediterranean, many works have shown that the parasitic fauna of this species of mullet is almost the same with an infestation rate that varies from one region to another, such as Bartoli et al. (1991), Bartoli et al. (2005), Martinez-Vicaria et al. (2000), Derbel et al. (2012), Anter et al. (2018) and Bottari et al. (2020) In the Mediterranean M. barbatus harbors a very limited number of parasites unlike the first species, our results are different from the works of Janiszewska (1953), Martinez-Vicaria et al. (2000), Derbel et al. (2012) and Bottari et al. (2020) and therefore we report the presence of D. latus for the first time in Algeria in M. barbatus, as well as L. excisum.

In the present study, both species of mullet have a high infestation with a significant difference between their prevalences. According to our results, O. furcatus is the most frequent and abundant species in both host fishes, which is similar to many works in the Mediterranean Sea; according to Derbel et al. (2012), Martinez-Vicaria et al. (2000), Bottari et al. (2020), several authors have reported the presence of the latter in different points of the Mediterranean, on the other hand, the latter is followed by P. furcatum, these results are in agreement with those obtained by Martinez-Vicaria et al. (2000) in Spain. On the other hand, Derbel et al. in 2012 and Bottari et al. in 2020 reported the same parasites except for P. furcatum in M. barbatus. In western Algeria, we found in M. surmuletus four species of parasites D. latus, O. furcatus, P. furcatum and P. bacilliovatum. These results are similar to the work of Brahim Tazi et al. (2009), Haddad et al. (2013) and Hassani et al. (2015); moreover, in our case, the infestation rate of D. latus is very high (P = 100 %, A = 1.00) in contrast to previous works (P = 4 %, A = 0.07; P = 1 %, A = 0.04; P = 8 %, A= 0.11 respectively), this may be due to either the availability of the intermediate host or the feeding regime.

It is also noted that the infestation rate of O. furcatus and P. furcatum is higher in M. surmuletus than in M. barbatus, which is similar to the work of Martinez-Vicaria et al. (2000) in Spain. On the other hand, the species O. furcatus is still dominant in M. surmuletus in the Mediterranean as Derbel et al. (2012), Hassani et al. (2015) and Bottari et al. (2020) contrary to the work of Bartoli et al. (2005) and Anter et al. (2018) where they reported that P. furcatum and P. bacilliovatum, respectively, have a high rate of infestation in comparison to the other parasite species.

This study also shows that the prevalence rate of parasites as a function of host size is always high in large fish compared to small fish in both host species; these results are similar to those of Martinez-Vicaria et al. (2000) where it was observed that the infestation rate of O. furcatus and P. furcatum is high in both large mullidae species. On the other hand, Martinez-Vicaria et al. (2000) indicate that there is no significant difference between parasitism and the size of the fishes, contrary to our data which show a highly significant difference between the infestation rate, the size and the weight of the hosts. Our results show that small fish are more parasitized than the big ones; this can be due to the immune system which is weak. Concerning parasitism, according to the seasons, we notice a significant difference contrary to Martinez-Vicaria et al. (2000). However, it is noted that O. furcatus is always more abundant throughout the year than P. furcatum which is similar to the work of Martinez-Vicaria et al. (2000) in Spain, according to Bartoli and Gibson (1991) the latter species has a lower prevalence and a more restricted distribution compared to O. furcatus, Moreover, it was deduced that in Algeria these two species of parasites are present during the four seasons in the two host species with a high infestation rate, unlike the species O. furcatus, which exists in Spain and has a low rate in autumn, on the other hand we note that the infestation rate of P. furcatum in Algeria in M. barbatus is low in winter and high in spring in M. surmuletus which differs from the work of Martinez-Vicaria et al. (2000) in Spain where the infestation rate is low in autumn in M. barbatus while it is high all year round in M. surmuletus This may be due to the variation in the diet of mullidae throughout the year (Derbal et al., 2010; El Bakali, 2010) or their feeding habits (Arculeo et al., 1997), although both fish species dig the substrate when feeding and use barbels to detect their prey but M. barbatus digs deeper in search of its prey than M. surmuletus. According to Derbal et al. (2010) the diet of the latter shows heterogeneity in spring and autumn and they considered that M. surmuletus is a voracious predatory species that feeds throughout the year, including during the period of gonad maturation which extends from February to June on the Algerian east coast.

It should be noted that the Correspondence Factorial Analysis (CFA) allowed us to link parasitism to seasons (Dajoz, 1982); it showed us that each parasite species has a high parasite specificity at a given period, unlike other digenean parasites, which are present all year round. However, unfortunately, we could not compare our data with other works because this test was done for the first time.