From 2009 to 2015, we examined sharks from off Algeria, mainly deep-sea species, for gill monogeneans. Only two species of gill monogeneans were collected, although ten species of sharks and 765 shark specimens were investigated. One was
Sharks were obtained from fishermen in Dellys (36° 55’ N; 3° 53’ E), Cap Djenet (36° 43’ N; 3° 36’ E), Bou Haroun (36° 40’ N; 4° 40’ E), and Cherchell (36° 37’ N; 2° 11’ E). All four localities are on the Mediterranean coast within 100 km near Algiers, Algeria and thus results are not detailed according to the localities. The following deep-sea shark species were examined for gill monogeneans from 2009 to 2015: gulper shark,
The gills were removed and observed in filtered seawater for mono-geneans. Monogeneans, located using a stereo-microscope were removed alive (dead for the few specimens from
We used a QIAmp DNA Micro Kit (Qiagen) to extract DNA. Eution was performed in 60μL. The specific primers JB3 (=COI-ASmit1) (forward 5'-TTTTTTGGGCATCCTGAGGTTTAT-3') and JB4.5 (=COI-ASmit2) (reverse 5'-TAAAGAAAGAACATAATGAAAATG-3') were used to amplify a fragment of the COI gene (Bowles
Among the 765 sharks examined over six years, belonging to ten species, only two species had monogeneans on their gills.
Our specimens were not in optimal state of conservation because these sharks were not fresh; however, the sclerotised parts could be observed and measured. Measurements (in parenthesis, measurements in Justine, 2011 for comparison): anterior sclerites 1,480 – 2,054 (1,680 – 1,720); median sclerites 1,850 – 2,498 (1,950 – 2,550); posterior sclerites 1,795 – 2,331 (1,820 – 2,330); hamulus outer length 89 – 96 (66 – 88); hamulus inner length 74 – 85 (70 – 85).
Type host:
Additional localities: Trieste (Italy) (Cerfontaine, 1899); Sète (France) (Maillard & Oliver, 1966; Euzet & Maillard, 1974); near Algiers (Algeria) (this paper).
Specimens examined: 7 specimens from 3 host fish.
Prevalence in Algeria: 100 % (3/3).
Material deposited: MNHN, slides HEL558.
Measurements of our specimens from Algeria are consistent with an identification with
Based on 32 specimens; measurements in Table 2, including separate measurements for holotype and means for all specimens. Body elongate, slender, haptor wider than body. Haptor symmetrical, armed with six suckers, each provided with hook-shaped sclerite, and appendix bearing single pair of terminal suckers and single pair of hamuli, each with one sclerite. Haptoral sclerites in 3 pairs arranged symmetrically, each with same shape and with point at right-angles to distal end of sclerite shaft; median sclerites slightly longer than those of anterior and posterior pairs. Appendix elongate, directed anteriorly in flattened specimens. Pair of hamuli with V-shaped root situated near distal end of appendix. Pair of terminal suckers oblong.
“Small” species of
Species | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Source | Cerfontaine, 1899 | Maillard, 1970 | Maillard, 1970 | Kitamura | This paper | Goto, 1894 | MacCallum, 1931 | Price, 1942 | Dillon | Martorelli et al., 2008 | Tendeiro | Maillard, 1966 |
Name in source | ||||||||||||
Host name in source | ||||||||||||
Host valid name | ||||||||||||
Locality | East Atlantic (Roscoff, France) | Mediterranean (Sète, France) | Mediterranean (Sète, France) | Pacific (Japan) | Mediterranean (Sète, France) MNHN 711 H, Ti 52 | Pacific (Japan) | Several | Atlantic (USA) | Pacific (New Zealand) | Atlantic (Argentina) | Indo-Pacific (Angola) | Mediterranean (Sète, France) |
n | 7 | 2 | 13 | 1 | several | 13 | 56 | 11 | 2 | 4 | ||
Total body length | 7,000 – 8,000 | 3,300 – 7,500 | 3,000 | 3,200 – 7,500 | 3,533 | 8,000 – 9,000 | 7,000 – 10,000 | 3,400 – 7,000 | 4,310 – 6,650 | 4,760 – 6,960 | 1,420 – 1,690 | 1,700 – 2,300 |
Body proper width | 1,000 – 1,500 | 350 | 500 – 1,200 | 407 | – | 1,500 | 765 – 935 | 620 – 1,060 | 62 – 87 | 680 – 690 | 330 – 450 | |
Anterior sucker diameter | 340 – 420 | 200 | 220 – 228 | 190 – 270 | 200 – 250 | |||||||
Length | 190 – 350 | 170 | ||||||||||
Width | 250 – 430 | 218 | ||||||||||
Pharynx diameter | 120 – 130 | 75 | 50 – 120 | |||||||||
Pharynx length | 120 | 70 – 120 | 130 | 84 – 117 | 57 – 67 | |||||||
Pharynx width | 60 | 60 – 120 | 122 | 61 – 69 | 40 – 60 | |||||||
Haptor length | 900 – 1,400 | 1,000 – 2,800 | 1,147 | 1,300 | 1,120 – 1,260 | 400 – 510 | 546 | |||||
Haptor width | 700 – 1,000 | 800 – 1,700 | 1240 | 830 – 1,250 | 600 – 660 | 336 | ||||||
Anterior sclerite length | 650 – 770 | 560 – 650 | 230 – 300 | 654 | 280 | 500 – 600 | 325 – 480 | 570 – 910 | 300 – 350 | |||
Median sclerite length | 680 – 800 | 580 – 690 | 230 – 300 | 683 | 280 | 500 – 600 | 366 – 480 | 570 – 910 | 290 – 360 | |||
Posterior sclerite length | 660 – 770 | 560 – 630 | 190 – 238 | 650 | 280 | 430 – 600 | 337 – 494 | 570 – 910 | 310 – 330 | |||
Appendix length | 400 | 800 – 1,900 | 537 | 765 – 935 | 641 – 925 | 740 – 1,350 | 440 – 450 | 300 – 370 | ||||
Appendix width | 200 | 250 – 500 | 185 | 255 – 340 | 100 – 210 | 200 – 220 | 200 – 230 | |||||
Hamulus length | 47 – 61 | 63 – 70 | 55 – 65 | 85 | 40 | 72 | 72 | 61 – 72 | 50 – 70 | 37.5 – 42.5 | ||
Hamulus outer length | 8 – 16 | 59 | 14 – 18 | |||||||||
Hamulus inner length | 15 – 23 | 61 | 12 – 14 | |||||||||
Testes number | 30 – 40 | 100 – 150 | 25 – 40 | 25 | 60 | 40 – 60 | 30 – 69 | numerous | few | |||
Cirrus bulb | ||||||||||||
Cirrus length | 650 | 350 | 200 – 370 | 75 – 100 | ||||||||
Cirrus width | 40 | 60 – 110 | 40 – 50 | |||||||||
Egg, proper length | 100 | 125 – 360 | 320 | 285 – 340 | 210 – 247 | 250 – 350 | 230 | 220 | ||||
Egg, filament number | 2 | 2 | 2 | 2 | 2; 50 – 60 | 2 | ||||||
Seminal receptacle length | ||||||||||||
Seminal receptacle length | 210 – 350 | 241 | 400 – 550 | |||||||||
Seminal receptacle width | 75 – 160 | 155 | 100 – 150 |
“Large” species of
Species | S. | S. | |||
---|---|---|---|---|---|
Source | Van Beneden, 1853 | Cerfontaine, 1899 | Yamaguti, 1958 | This paper | This paper |
Name in original description | |||||
Host name in original description | |||||
Host valid name | |||||
Locality | Atlantic, North Sea (Belgium) | Atlantic, North Sea (Belgium) | Pacific (Japan) | Mediterranean (Algeria) | Mediterranean (Algeria) |
n | 6 | 5 | Holotype | 31 paratypes | |
Total body length | 25,000 – 30,000 | 20,000 (unflattened) | 8,500 – 14,000 | 18,463 | 12,921±3,289 (7,326 – 21,830, n=32) |
Body proper width | 3,000 – 4,000 | 1,200 – 1,400 | 1,628 | 1,078±239 (777 – 1,813, n = 32) | |
Anterior sucker diameter | 310 – 390 | ||||
Anterior sucker length | 306 | 286 (201 – 410, n = 20) | |||
Anterior sucker width | 366 | 343 (261 – 448, n = 20) | |||
Pharynx diameter | 70 – 110 | ||||
Pharynx length | 194 | 179 (112 – 246, n = 21) | |||
Pharynx width | 149,2 | 164 (119 – 216, n = 21) | |||
Haptor length | 4,051 | 2,428 (1,758 – 4,051, n = 12) | |||
Haptor width | 3,552 | 2,450 (1,610 – 3,552, n = 12) | |||
Anterior sclerite length | 2,228 From measurements on drawings | 750 – 920 | 1,638 | 1,763 (1,130 – 2,906, n = 20) | |
Median sclerite length | 600 – 620 | 1,675 | 1,851 (1,171 – 2,909, n = 20) | ||
Posterior sclerite length | 600 – 620 | 1,586 | 1,749 (1,089 – 2,738, n = 20) | ||
Appendix length | 800 – 1,100 | 1,029 | 872 (522 – 1,186, n = 10) | ||
Appendix width | 400 – 530 | 306 | 207 (142 – 336, n = 10) | ||
Hamulus length | 40 – 50 | ||||
Hamulus outer length | 83 From measurements on drawings | 87 | 70 (59 – 87, n=13) | ||
Hamulus inner length | 66 From measurements on drawings | 74 | 63 (44 – 74, n = 13) | ||
Testes number | numerous | 100 or more | 82 | 82 (69 – 96, n = 10) | |
Cirrus length | 130 – 150 | 307 | 421 (307 – 551, n = 7) | ||
Cirrus width | 120 – 150 | ||||
Eggs proper length | 250 | 450 | 539 (463 – 644, n = 5) | ||
Egg filament number and length | 2; 100 – 150 | 2 | |||
Seminal receptacle length | 250 – 420 | 410 | 667 (522 – 858, n = 11) |
Anterior sucker terminal. Pharynx subspherical. Oesophagus short. Caeca internally moderately diverticulate, confluent in posterior part of body, end as two short caeca, one which extends into haptor and one into appendix.
Testes numerous, occupy intercaecal area of posterior part of body, end posteriorly before confluence of caeca. Single sperm duct (vasa efferentia) well visible from testes to seminal vesicle. Seminal vesicle, begins just anterior to oötype, convoluted, thinwalled, contains spermatozoa, continues anteriorly and connects with cirrus; no posterior lobe. Cirrus elongate, unarmed, connects with genital atrium. Prostatic glands not seen. Genital atrium ventral, median, just posterior to bifurcation of caeca.
Ovary located at mid-length of body proper; proximal part of ovary slightly branched; descending and ascending ovarian parts straight; ovary terminates as slender canal superposed to seminal receptacle. Connections of terminal ovary, anterior part of seminal receptacle, posterior part of ovovitelloduct, posterior part of median vitelloduct and genitointestinal canal apparently all located just anteriorly to seminal vesicle. Ovovitelloduct convoluted, without diverticulum, connects anteriorly with oötype. Seminal receptacle cylindrical, oblique with anterior connection. Two lateral vitelloducts unite to form posteriorly directed median vitelloduct, with coil. Oötype wall with longitudinal rows of large cells (‘oötype côtelé’ of Euzet and Maillard 1974). Mehlis’ glands surround oötype. Oötype anteriorly joins uterus. Uterus straight, contains few eggs, ends anteriorly in genital atrium. Two vaginal openings, located just posteriorly to genital atrium or at the same level; anterior portion of vaginae often widened, filled with spermatozoa; posterior portion not well visible.
Eggs fusiform, elongate, operculum not seen, with two polar filaments.
We obtained COI sequences, 396 bp in length, for three specimens; the sequences differed between them by 4 and 6 nucleotide (1 – 1.5 %). A GenBank BLAST of the sequences showed that the closest species were polystomatid polyopisthocotylean monogeneans. These sequences were widely different (20 – 30 %) as polystomatids and hexabothriids are not closely related family. COI sequences are generally appropriate for distinguishing species; in the absence of any other sequence of hexabothriid monogeneans in databases, further comments are useless. Our sequences of
Type-host:
Additional localities: Off Cap Djenet (36° 43’ N; 3° 36’ E), off Bou Haroun (36° 40’ N; 4° 40’ E), off Cherchell (36° 37’ N; 2° 11’ E), Algeria; all these localities are within 100 km of Algiers.
Site of infection: gills
Comparative material observed: One slide of
Etymology: named in honour of Professor Louis Euzet, famous parasitologist and author of major works on hexabothriids, who examined the specimens and confirmed their interest.
Species included in
Species attributed to
Boeger & Kritsky (1989) included only four species in the genus:
Kitamura et al. (2006) apparently followed Boeger & Kritsky (1989) when they considered their new species
The list of species of
We provide here a few remarks about
The characteristic oötype with longitudinal rows of cells (‘oötype côtelé’ of Euzet and Maillard, 1974) is found only in three hexabothriid genera, including
In the following discussion, we do not consider
We found that species of
The family Hexabothriidae has been the focus of several revisionary works, including a revision with historical account (Euzet & Maillard, 1974) and a revision associated with a cladistic analysis (Boeger & Kritsky, 1989). The number of genera included in the family has slowly increased from eleven (Euzet & Maillard, 1974) and thirteen (Boeger & Kritsky, 1989) to a total of fifteen in most recent works (Patella & Bullard, 2013). However, the hexabothriid literature is plagued with confusion and discrepancies (Vaughan & Christison, 2012) but probably no more than any large family of monogeneans. The Hexabothriidae are considered a basal group within the Polyopisthocotylea in phylogenies based on morphology (Boeger & Kritsky, 1993) and molecules (Mollaret
Our study also emphasizes the very small number of molecular sequences available for members of this family – so far, our COI sequence of