First Record of Schilbetrema (Monopisthocotyla: Dactylogyridae) from Schilbe depressirostris in South Africa

Abstract

The study presents a survey of monopisthocotylan parasites infecting Schilbe depressirostris in the northern region of South Africa. Fish specimens were collected from five different localities and examined for gill-infesting monopisthocotylans. To date, there have been no records of monopisthocotylans associated with this host species in South Africa. Across Africa, fourteen monopisthocotylan species of the genus Schilbetrema and two species of Schilbetrematoides have been reported from schilbeid hosts. In the present study, three species of Schilbetrema were identified, each showing varying levels of infestation: Schilbetrema quadricornis was found at all five localities; Schilbetrema acornis was recorded at four localities; and Schilbetrema undinula was detected at a single locality. Seasonal variation in infestation was not significant; however, infestation was positively correlated with host size.

1. Introduction

Schilbe depressirostris (Peters, 1844) commonly known as the Eastern butter catfish is a member of the butter barbel family, Schilbeidae (Osteichthyes: Siluriformes) with Schilbe Oken, 1817 being endemic to tropical African waters. This species was previously grouped with other African schilbeids; however, it was recently reinstated as distinct from Schilbe intermedius Rüppell, 1832 based on both morphological and molecular data [1,2]. As a result, S. depressirostris was recently still referred to as S. intermedius, and caution is therefore advised when interpreting historical parasite records. Schilbeid fishes are known to host a variety of gill parasites, particularly species belonging to the African Dactylogyridae. The first dactylogyrid genus, Schilbetrema Paperna and Thurston, 1968 was described by Paperna & Thurston [3] from the host Schilbe mystus (Linnaeus, 1758) in Uganda. Subsequently, a number of authors described and recorded Schilbetrema spp. from Ghana [4,5], Tanzania [5], Egypt [6], Togo [7], Zimbabwe [8] and the Ivory Coast [9]. This genus now includes 14 species, all from schilbeid hosts. A second genus, Schilbetrematoides Kritsky and Kulo, 1992, was described from S. intermedius in Togo by Kritsky & Kulo [10], whereafter N’douba et al. [11] added a second species to this genus from Schilbe mandibularis (Guenther, 1867) in the Ivory Coast. Parasite records from this host in South Africa are limited to endoparasites and represented by Smit et al. [12], Smit & Luus-Powell [13], Tavakol et al. [14] and King et al. [15]. This study aimed to document the diversity and host associations of monopisthocotylan species infecting S. depressirostris in South Africa, providing the first national record of the genus and contributing to knowledge of parasite biodiversity in the region.

2. Materials and Methods

Schilbe depressirostris specimens were collected seasonally between 2009 and 2015 from five different localities in the northern region of South Africa using gill nets. The Nwanedi-Luphephe and Nandoni dams forms part of the Limpopo River System, and Flag Boshielo and Loskop dams, as well as the Phalaborwa Barrage, are found in the Olifants River System. The hosts (Nwanedi-Luphephe Dam, n = 60; Nandoni Dam, n = 89; Loskop Dam, n = 60; Flag Boshielo Dam, n = 65; and the Phalaborwa Barrage, n = 60) were examined for gill parasites with the aid of a stereo microscope (LEICA Microsystem, model EZ4, Wetzlar, Germany). Monopisthocotylans were removed from the gill filaments using fine forceps and entomological needles and mounted on slides using glycerine jelly or ammonium picrate–glycerine (GAP), as documented by Malmberg [16].

Line drawings were made freehand with the aid of a drawing tube connected to a Zeiss Axioplan 2 imaging microscope (Jena, Germany), and geometric analysis of selected specimens was performed. The sclerotised parts were photographed and measured using the same microscope, making use of Axiovision 4.7.2 software. Measurements were taken as proposed by Gussev [17] and given in µm (mean and range). Monopisthocotylan species were identified using the morphological features of the haptoral sclerites following Kritsky & Kulo [7].

The prevalence, mean abundance and mean intensity of the different species were calculated following standard parasitological descriptions, as defined by Bush et al. [18]. Females were larger and dominant, with a sex ratio of 4.2:1. Because of this disproportionate sex ratio, the influence of host sex on parasitic burden was ignored. Seasonal variation in infestation was calculated to determine if any significant differences occurred. May to August were considered as winter (low flow) and September to April as summer (high flow). Fish hosts were divided into three length groups (<16 cm, 16–25 cm and >25 cm) according to their standard lengths. These length groups were determined by Smit & Luus-Powell [13] using the growth curve constructed by Hecht [19] for S. depressirostris (previously known as Eutropius depressirostris) from Nwanedi-Luphephe Dam. Standard lengths less than 16 cm correspond with fish of 2 years and younger, 16 to 25 cm with fish between 2 and 4 years, and those with lengths longer than 25 cm, with fish older than 4 years. The Spearman’s rank correlation coefficient (r_s) was used to correlate fish size (SL) with intensity of infection. The Kruskal–Wallis test was employed to determine significant differences in the intensity of infection during the different seasons, as well as between the different fish length groups. All p-values less than 5% (p < 0.05) were considered significant.

3. Results and Discussion

Monopisthocotylans recovered from the gills of Schilbe depressirostris during this study resulted in three dactylogyrid species, morphologically corresponding to Schilbetrema, as described by Paperna & Thurston [3] and Kritsky & Kulo [7]. Characteristics of the haptoral parts define the genus and include the presence of a prominent superficial knob on the ventral anchor base near its union with the shaft; a modified ventral anchor with a short to non-existent shaft, an elongate point and compressed basal roots; ventral and/or dorsal haptoral bars with lateral, subterminal and/or submedial anterior projections; and hooks with protruding thumbs and slender shanks.

The ventral bar was the most profound feature used to differentiate among the Schilbetrema spp. collected during this study. The ventral bar of Schilbetrema quadricornis Paperna and Thurston, 1968 is long, with two bilateral horns and a delicate submedial projection without terminal ornamentation (Figure 1A and Figure 2). In Schilbetrema acornis Paperna and Thurston, 1968, this structure is shorter and stumpy, lacking terminal horns and having a flabby and bilaterally flattened submedial projection (Figure 1B and Figure 3). The ventral bar of Schilbetrema undinula Kritsky and Kulo, 1992 has short terminal horns and a simple anteromedial process (Figure 1C and Figure 4). It can thus be difficult to differentiate between S. acornis, S. undinula and even S. aegyptica. However, the ventral bar of S. acornis is short and stumpy whereas this structure is comparatively slender in S. undinula and is broad and flattened in S. aegyptica [6,7]. Specimens collected from the different localities were examined and measurements of whole worms and haptoral sclerites are presented in

Table 1. Measurements of the body and sclerotised haptoral features (mean, minimum and maximum values given in µm) of Schilbetrema quadricornis from the current study compared to available data for this species.

Measurements from Schilbetrema quadricornis	Paperna &Thurston [3] (Type Specimens)	Kritsky & Kulo [7] (Redescription)	Douëllou & Chishawa [8]	Current Study (n = 10)
Body length	439 (364–514)	401 (309–513)	500 (340–590)	436.0 (316.0–530.0)
Body width	146 (138–153)	74 (56–89)	68 (40–88)	80.3 (69.0–105.0)
Haptor length	85 (78–93)	82 (71–102)	-	82.5 (72.0–100.0)
Haptor width	82 (81–83)	73 (61–85)	-	76.3 (68.0–83.0)
Dorsal anchor length	54 (52–55)	59 (52–65)	61.1 (55.0–64.6)	58.2 (53.0–63.0)
Dorsal anchor base width	23 (20–26)	22 (17–26)	-	22.0 (19.2–25.0)
Dorsal bar length	39 (38–40)	39 (36–45)	38.4 (35–41)	40.0 (37.4–43.0)
Ventral anchor length	23 (22–25)	25 (21–28)	20.8 (19.9–22.5)	23.1 (20.0–25.9)
Ventral bar length	40 (40)	40 (36–47)	41 (36.4–45.9)	41.7 (37.0–45.3)
Marginal hook length	15–16	17 (16–18)	13.2–17.4	15.9 (14.0–17.5)

,

Table 2. Measurements of the body and sclerotised haptoral features (mean, minimum and maximum values given in µm) of Schilbetrema acornis from the current study compared to available data for this species.

Measurements from Schilbetrema acornis	Paperna &Thurston [3] (Syntype Specimens)	Kritsky & Kulo [7] (Redescription)	Current Study (n = 10)
Body length	577	430 (333–568)	434.0 (380.0–540.0)
Body width	149	94 (68–118)	96.4 (75.0–121.0)
Haptor length	87	61 (56–66)	62.8 (58.0–67.0)
Haptor width	99	62–63	62.8 (62.1–64.0)
Dorsal anchor length	37–38	35 (34–37)	36.0 (35.0–38.0)
Dorsal anchor base width	15 (13–17)	15–16	15.1 (14.8–16.5)
Dorsal bar length	23	27 (23–31)	27.8 (24.0–31.2)
Ventral anchor length	26–27	28 (26–30)	28.2 (26.5–30.1)
Ventral bar length	20	19 (18–22)	19.8 (18.3–22.6)
Marginal hook length	23	20–22 and 23–27	24.1 (20.0–27.2)

and

Table 3. Measurements of the body and sclerotised haptoral features (mean, minimum and maximum values given in µm) of Schilbetrema undinula from the current study compared to available data for this species.

Measurements from Schilbetrema undinula	Kritsky & Kulo [7] (Species Description)	Douëllou & Chishawa [8]	Current Study (n = 6)
Body length	281 (233–314)	590 (400–840)	575.0 (465.0–655.0)
Body width	77 (50–102)	90 (70–120)	87.0 (79.0–96.0)
Haptor length	53 (52–55)	–	53.4 (52.2–54.2)
Haptor width	58 (50–65)	–	58.0 (53.0–62.0)
Dorsal anchor length	33 (29–36)	31.8 (27.2–34.8)	31.9 (28.5–35.0)
Dorsal anchor base width	15 (13–17)	–	15.7 (15.1–16.2)
Dorsal bar length	26 (23–29)	24.5 (23.2–25.7)	25.6 (24.2–28.3)
Ventral anchor length	23 (21–26)	21.5 (18.2–24.8)	22.1 (20.5–24.0)
Ventral bar length	29 (26–35)	22.9 (21.5–24.0)	23.0 (22.4–23.8)
Marginal hook length	18–19 and 20–21	21.5 (18.0–24.0)	20.1 (18.0–23.1)

. The measurements are compared with available morphometric data for the respective species reported by Paperna [3], Kritsky & Kulo [7] and Douëllou & Chishawa [8].

Notable differences were observed in the distribution of Schilbetrema spp. among the sampling localities, along with variation in the intensity of infestation (

Table 4. The prevalence, mean abundance and mean intensity of monopisthocotylans recorded from Schilbe depressirostris from five localities in South Africa.

	Schilbetrema  quadricornis	Schilbetrema  acornis	Schilbetrema  undinula
Nwanedi-Luphephe Dam	83.3%; 20.3; 21.3	25.0%; 1.5; 6.0	–
Nandoni Dam	94.4%; 45.9; 48.6	–	–
Loskop Dam	96.7%; 39.7; 41.0	28.3%; 4.8; 16.8	–
Flag Boshielo Dam	90.8%; 11.2; 12.3	69.2%; 4.1; 5.9	–
Phalaborwa Barrage	85.0%; 10.6; 12.5	70.0%; 8.3; 11.9	13.3%; 0.5; 3.8

Prevalence; mean abundance; mean intensity.

). Schilbetrema quadricornis was the dominant species, with a prevalence of >83.3%, and was recorded at each of the studied localities. The prevalence of S. acornis varied between the localities (25.0–70.0%) and was not recorded from Nandoni Dam. Schilbetrema undinula was only recorded from the Phalaborwa Barrage (prevalence = 13.3%). Some of the hosts were highly infested with Schilbetrema spp. (e.g., 339, 346 and 480 worms from individual host specimens at Nandoni Dam) which might have had a negative effect on the condition of those specific hosts.

The variation in physicochemical conditions measured among the study localities did not adequately explain the observed differences in Schilbetrema spp. distribution. However, Nandoni Dam, which was the only locality where the fish host harboured a single Schilbetrema species, is the youngest of the study localities and is hydrologically isolated, with the Luvuvhu River joining the Limpopo River more than 100 km downstream. The Phalaborwa Barrage, the only locality at which S. undinula was recorded, is characterised by high turbidity and pronounced seasonal variation in flow, in contrast to the other localities, which are more static impoundments. Broader environmental variation, including differences in flow regime, turbidity and seasonal hydrological instability, may drive local adaptation in parasites, particularly in attachment and reproductive structures [20,21]. These conditions may impose stronger selective pressures that favour parasite species adapted to dynamic riverine environments, which might explain the additional monopisthocotylan species at this locality.

The standard length (SL) of fish hosts collected ranged from 11.2 to 34.0 cm and the weight from 16.0 to 587.0 g. Female fish recorded were significantly (p ≤ 0.05) larger than males, and each size group was well represented. The data from for all localities were pooled and the prevalence, mean abundance and mean intensity of Schilbetrema spp. for each fish length group calculated. Fish belonging to the smallest, medium and largest length groups had calculated indices of 91.1%, 22.8, 25.0; 92.8%, 40.3, 43.4 and 95.9%, 44,1, 46.0, respectively, indicating all indices increased with fish size. The intensity of Schilbetrema spp. infestation was compared to the standard length of the host by using Spearman’s rank correlation coefficient (r_s) and approached significance (p = 0.055; r_s = 0.295). Larger fish therefore tended to harbour more monopisthocotylans. This is in agreement with a number of other studies on monopisthocotylan fish parasites [22,23].

Seasonal fluctuations in Schilbetrema spp. infestation are presented in

Table 5. Seasonal prevalence, mean abundance and mean intensity of Schilbetrema spp. recorded from Schilbe depressirostris from five localities in South Africa.

	Winter	Summer
Nwanedi-Luphephe Dam	93.3%; 41.3; 44.3	90.0%; 29.8; 33.1
Nandoni Dam	92.5%; 36.3; 39.2	95.0%; 47.9; 50.4
Loskop Dam	98.3%; 47.0; 47.7	96.7%; 45.6; 47.1
Flag Boshielo Dam	91.7%; 18.7; 20.3	95.4%; 24.9; 26.1
Phalaborwa Barrage	93.3%; 54.7; 58.6	95.0%; 59.4; 62.6

Prevalence; mean abundance; mean intensity.

. Although temperature plays a role in monopisthocotylan life cycles, a number of studies indicate no correlation between temperature and prevalence/mean abundance of monopisthocotylans [24,25,26]. This was evident in the current study with little variation in infestation levels of Schilbetrema spp. between winter and summer for most localities. It is most likely that this tendency is because the studied localities are all located within a temperate region where water temperature during winter does not drop to levels that are unfavourable for these monopisthocotylan species. However, the mean abundance recorded from Flag Boshielo Dam was significantly higher during summer (p ≤ 0.05), although no specific contributing factors could be identified.

4. Conclusions

This study increases the current knowledge of monopisthocotylans from S. depressirostris, and reports, for the first time, Schilbetrema spp. in butter catfish from South Africa. These findings are valuable to science and add relevant information on the distribution and ecology of African dactylogyrids. It is suggested that molecular data should be obtained as the only available records are from an unidentified Schilbetrema sp. (GenBank ID KP056243–44) collected from Pareutropius debauwi (Boulenger, 1900) residing in an aquarium. It is further suggested that the morphology of these monopisthocotylans should be compared to Schilbetrema spp. recorded from the rest of Africa to determine if these species are similar to the known species or if they co-evolved with the specific host.