Carrassoniella Dallarés & Schaeffner, 2025

Dallarés, Sara, Barría, Claudio F. & Schaeffner, Bjoern C., 2025, Integrative taxonomy in action: a new genus of phyllobothriid tapeworms (Cestoda: Phyllobothriidea), with insights on potential transmission pathways and influences of environmental gradients on diversity paterns of the group, Zoological Journal of the Linnean Society 204 (1) : -

Genus Carrassoniella Dallarés & Schaeffner gen. nov.

ZooBank registration: urn:lsid:zoobank.org:act:FDCE8600-401A-4AB6-9C73-FB8EA27570F5

Type species: Carrassoniella sinuosiceps ( Williams, 1959) comb. nov.

Etymology: Tis genus honours Dr Maite Carrassón, who has made vast contributions to the knowledge on the biology, ecology, and parasitology of Mediterranean deep-sea fishes.

Generic diagnosis

Worms apolytic, craspedote. Scolex subspherical, foliose; cephalic peduncle and myzorhynchus lacking; neck scutellate. Bothridia uniloculate, not distinctly divided, crenulated, with large subdivided folds and frilled edges, with small apical suckers at apex. Scolex spinitriches gongylate columnar and trullate on distal and proximal bothridial surfaces, respectively, interspersed with acicular filitriches. Strobila filitriches capilliform. Immature, mature, and gravid proglotids wider than long. Testes numerous, medullary, oval, absent in post-ovarian field. Vas deferens coiled. Genital pores lateral, irregularly alternating; genital atrium shallow; lip-like structures surrounding genital pore. Cirrus sac narrowly oblong, slightly curved anteriorly, containing armed cirrus; cirrus with spinitriches, everts into vagina of same proglotid, dilated distally. Vagina weakly sinuous, extending from ootype along midline of proglotid to anterior margin of vas deferens, then laterally along anterior margin of cirrus sac towards genital atrium, dilated in distal region; vaginal sphincter absent; seminal receptacle present. Ovary terminal, H-shaped in frontal view; ovarian isthmus in posterior part. Mehlis’ gland posterior to ovarian isthmus. Uterus medial, ventral to vagina, saccate, extending from ovarian isthmus to posterior margin of cirrus sac; uterine pore absent. Vitellarium follicular; follicles in two lateral bands; vitelline bands extending throughout length of proglotid, partly or fully interrupted by terminal genitalia, uninterrupted by ovary. Excretory vessels in two lateral pairs, arranged in a dorsal and ventral pair. Intrauterine eggs fusiform, unembryonated. Parasites of cowsharks ( Hexanchiformes : Hexanchidae ). Distribution in the north-eastern Atlantic waters, including the Mediterranean Sea, and the southwestern Pacific.

Remarks

With the erection of Carrassoniella , 22 phyllobothriid genera are considered valid. Te genus is characterized by a highly foliose, spherical scolex with indistinctly demarcated bothridia, which are crenulated and bear large folds and frilled edges. Tis scolex appearance differentiates the new genus from nearly all phyllobothriid genera. Five genera, or members thereof, possess foliose or highly folded bothridia, viz. Clistobothrium Dailey & Vogelbein, 1990 (viz. three species), Phyllobothrium , Rockacestus , Ruhnkebothrium , and Tysanocephalum Linton, 1890. However, the bothridia of members of all these genera are clearly demarcated and further differ in additional morphological features. Members of Ruhnkebothrium and Tysanocephalum have biloculate bothridia with an anterior loculus and a posterior foliose loculus. Te three members of Clistobothrium [i.e. Clistobothrium gabywalterorum Caira, Hayes & Jensen, 2020 , Clistobothrium montaukensis Ruhnke, 1993 , and Clistobothrium tumidum (Linton, 1922) ] have uniloculate bothridia with an apical sucker and usually a dome-shaped apical region. Members of Rockacestus have moderately to highly folded bothridia with an apical sucker but also marginal loculi, a feature absent in Carrassoniella . All three members of Phyllobothrium , viz. Phyllobothrium lactuca , Phyllobothrium riseri Ruhnke, 1996 , and Phyllobothrium serratum Yamaguti, 1952 , possess highly foliose bothridia with apical suckers. Tis bothridium appearance is morphologically similar to Carrassoniella ; however, the new genus lacks the bifid posterior extensions characteristic for members of Phyllobothrium .

Carrassoniella further differs from other phyllobothriid genera insurfaceultrastructuralfeatures.Manygeneraofphyllobothriids possess a scutellate strobila, whereas the scutes of Carrassoniella are restricted to the neck region. Tis morphological characteristic is shared with only the three species of Aleoandercestus Ruhnke& Workman, 2013.Inaddition, Carrassoniella possessesa unique combination of scolex microtriches. Te distal bothridial surface is lined with gongylate columnar spinitriches interspersed with acicular filitriches, whereas the proximal bothridial surface is covered by trullate spinitriches and acicular filitriches. Only a subset of members of three genera, viz. Orygmatobothrium Diesing, 1863 (three species), Scyphophyllidium Woodland, 1927 (14 species), and Yamaguticestus (two species), display gongylate columnar spinitriches on the distal bothridial surface. Yet, instead of trullate spinitriches, the proximal bothridial surface is lined by trifid- ( Orygmatobothrium ), gladiate, or serrate gladiate spinitriches ( Scyphophyllidium ) or acicular/capilliform filitriches ( Yamaguticestus ).

Another difference of Carrassoniella to other genera of phyllobothriids is the number of testes. Te range of testes presented by species appears to follow generic trends. With the exception of certain genera (viz. Bilocularia , Monorygma , Pelichnibothrium Monticelli, 1889 , Phyllobothrium , and Tysanocephalum), for which testes numbers have not been recorded, other genera generally present <100 (viz. Calyptrobothrium, Fleoibothrium McKenzie & Caira, 1998 , and Trilocularia ), 200 (viz. Bibursibothrium McKenzie & Caira, 1998 , Cardiobothrium McKenzie & Caira, 1998 , Guidus , Hemipristicola Cutmore, Teiss, Bennet & Cribb, 2011 , Rockacestus , and Scyphophyllidium ), 300 (viz. Clistobothrium and Ruhnkebothrium ), 400 (viz. Aleoandercestus and Yamaguticestus ), or <500 testes (viz. Orygmatobothrium ). Members of Crossobothrium do not follow this general trend for testes numbers of other phyllobothriid genera. Of the three species for which testes numbers have been reported, two species (i.e. Crossobothrium laciniatum Linton, 1889 and Crossobothrium pequeae Ivanov, 2009 ) possess <300 testes, whereas the testis number of Crossobothrium antonioi Ivanov, 2009 ranges between 692 and 771. Excluding genera for which testes numbers remain unknown, Crossobothrium antonioi represents the phyllobothriid species with the most testes in mature proglotids. With an average of 560 testes, Carrassoniella has a higher number of testes than all other phyllobothriid genera, but ~100 testes fewer than Crossobothrium antonioi . Apart from the above-mentioned characteristics, Carrassoniella can be distinguished readily from other phyllobothriid genera by the large size, apolytic state, presence of uniloculate bothridia, and absence of a vaginal sphincter.

Members of most phyllobothriid genera infect host species belonging to the same genus (i.e. Aleoandercestus, Guidus , Monorygma , Orygmatobothrium , Ruhnkebothrium , and Trilocularia ) or family (i.e. Calyptrobothrium and Phyllobothrium ). Six monotypic phyllobothriid genera are oioxenous, infecting a single host species ( Bibursibothrium , Cardiobothrium , Carrassoniella, Fleoibothrium , Hemipristicola , and Pelichnibothrium ). Other monotypic genera infect hosts of different families ( Bilocularia ) and even orders (Tysanocephalum). With 45 valid members, the species-rich genus Scyphophyllidium infects a broad array of carcharhiniform-, lamniform-, and orectolobiform sharks and even one representative of potamotrygonid stingray. Although most phyllobothriids tend to infect a rather narrow host spectrum, co-infections of other phyllobothriid species in the same host species are possible. Carrassoniella infects a single species of cowsharks (family Hexanchidae ). Tis shark family forms the predominant host group of the phyllobothriid genus Crossobothrium . Of the five valid species of Crossobothrium , four infect cowsharks, including the type host species of Carrassoniella , and a single species has been recorded from a carchariid shark.

Species Carrassoniella sinuosiceps ( Williams, 1959) , comb. nov.

( Figs 2, 3)

ZooBank registration: urn:lsid:zoobank.org:act:D3BDB03E-F7F6-4802-A25B-48BDCB6BE7FE

Synonyms

Phyllobothrium sinuosiceps Williams, 1959 .

Material examined

Holotype: NHM 1959.10.14.1/2. Specimen on two microscope slides (scolex, neck region, and parts of the immature strobila on slide 1; detached, gravid segment on slide 2).

Non-type material: SPAIN: Palamós , Balearic Sea; two complete mature specimens: one whole mount of a fully relaxed specimen (hologenophore sensu Pleijel et al. 2008) ( NHM accession number 2024.10.17.1-6), one specimen observed with scanning electron microscopy ( MNHG accession number MHNG-PLAT-0159627) .

Type and only host: Bluntnose sixgill shark, Heoanchus griseus ( Hexanchiformes : Hexanchidae ).

Type locality: Celtic Sea (North Atlantic Ocean), off the Irish coast (54°0′N, 11°15′W) .

Additional localities: Porcupine Bank ( North Atlantic Ocean ), off Ireland (coordinates unknown); Strait of Messina ( Tyrrhenian Sea ), off Torre Faro, Italy (38°15′52.8″N, 15°39′04.3″E); Chonos Archipelago (Southeastern Pacific Ocean), off Chile (coordinates unknown); Balearic Sea, Palamós (beach), Spain (41°50′37″N, 03°06′44″W) .

Site and infection parameters: Spiral intestine. Prevalence 100% (one shark in Spain and one in Italy); intensity of five or six worms per host, respectively.

GenBank accession number: Hologenophore ( NHM 2024.10. 17.1-6): PP937541 (28S).

Conservation assessment: Near Treatened [conservation assessment methodology for animal parasites ( CAMAP) criterion 6].

Redescription

[Based on two complete specimens: one whole mount of a fully relaxed, adult specimen (hologenophore) and one adult specimen observed with scanning electron microscopy.] Worms apolytic, slightly craspedote, 566.36 mm long (N = 1) ( Fig. 2B), with 1547 (N = 1) proglotids; maximum width at level of late immature proglotids, 4521 (N = 1) wide. Scolex spherical, foliose ( Figs 2A, 3A), 2809 (N = 1) long, 4213 (N = 1) wide, lacking apical organ.Bothridia uniloculate, not distinctly divided, crenulated, with large subdivided folds and frilled edges ( Figs 2A, 3A), 2591–2610 (N = 2) long, 2021–2089 (N = 2) wide; apical suckers present ( Figs 2A, 3A, B), four in number, 201–267 (224 ± 29; N = 4) long, 334–361 (344 ± 13; N = 4) wide, situated on apical fold on apex of scolex, covered with papilliform filitriches ( Fig. 3D), with row of tegumental pores on outer surface ( Fig. 3C). Distal bothridial surface covered with gongylate columnar spinitriches interspersed with acicular filitriches ( Fig. 3G); gongylate columnar spinitriches 1.6–2.3 (1.9 ± 0.2; N = 20) long, 0.3–0.5 (0.4 ± 0.1; N = 20) wide. Proximal bothridial surface covered with trullate spinitriches interspersed with acicular filitriches ( Fig. 3H), 1.0–1.3 (1.2 ± 0.1; N = 20) long, 0.3–0.5 (0.4 ± 0.1; N = 20) wide at base. Strobila covered with capilliform filitriches ( Fig. 3F).

Cephalic peduncle lacking. Neck 53.06 mm (N = 1) long, 1952 (N = 1) wide posterior to scolex, scutellate ( Fig. 3E). Immature proglotids wider than long, 1399 (N = 1) in number; early immature proglotids 171–240 (196 ± 27; N = 11) long, 2809–2980 (2880 ± 47; N = 11) wide, length-to-width ratio 12.1–17.4:1 (14.9 ± 2.0; N = 11); late immature proglotids 617–822 (691 ± 63; N = 11) long, 4076–4521 (4331 ± 120; N = 11) wide, length-to-width ratio 5.3–7.1:1 (6.3 ± 0.5; N = 11). Mature proglotids wider than long, 86 in number (N = 1); early mature proglotids 754–925 (866 ± 53; N = 11) long, 3905–4316 (4066 ± 112; N = 11) wide, length-to-width ratio 4.2–5.7:1 (4.7 ± 0.4; N = 11); late mature proglotids 1199–1610 (1,423 ± 133; N = 11) long, 3425–3905 (3634 ± 146; N = 11) wide, length-to-width ratio 2.2–3.1:1 (2.6 ± 0.3; N = 11) ( Fig. 2E). Gravid proglotids wider than long, 62 (N = 1) in number, 1439–1747 (1551 ± 92; N = 11) long, 3528–3870 (3665 ± 112; N = 11) wide, length-to-width ratio 2.1–2.6:1 (2.4 ± 0.2; N = 11).

Testes medullary, oval ( Fig. 2D, E), 80–127 (98 ± 8; N = 45) long, 67–87 (77 ± 5; N = 45) wide, in three layers, 544–581 (563 ± 17; N = 5) in number, arranged in 140–155 (148 ± 6; N = 5) preporal, 123–131 (127 ± 3; N = 5) postporal, and 274–302 (287 ± 12; N = 5) aporal testes, extending anteriorly from anterior margin of ovary to anterior margin of proglotid. Cirrus sac narrowly oblong, slightly curved anteriorly ( Fig. 2D, E), 1336–1884 (1625 ± 148; N = 20) long, 274–411 (356 ± 32; N = 20) wide, occupying 43.0%–56.3% (50.5% ± 3.9%; N = 20) of proglotid width, containing cirrus; cirrus with short spinitriches, distally dilated, everts into vagina of same proglotid ( Fig. 2D, E). Vas deferens coiled, extending anteriorly from anterior margin of cirrus sac ( Fig. 2D, E).

Genital pores lateral ( Fig. 2D, E), irregularly alternating, 50.0%–61.4% (55.8% ± 2.8%; N = 20) of proglotid length from posterior end; genital atrium shallow ( Fig.2D, E); muscular bulge present, forming external labial structures narrowing genital passage ( Fig. 3I). Vagina thin walled, weakly sinuous ( Fig. 2D), extending along median line anteriorly from Mehlis’ gland to anterior extent of vas deferens, 27–53 (42 ± 8; N = 20) in diameter, widening along anterior margin of cirrus sac towards genital atrium; dilated vagina 160–201 (183 ± 12; N = 20) in diameter, containing cirrus in proximal portion ( Fig. 2D), entering genital atrium anterior to cirrus sac; vaginal sphincter absent. Ovary symmetrical, lobulated, near posterior end of proglotid ( Fig. 2E), H-shaped in frontal view, 308–480 (379 ± 40; N = 20) long, 1576–1918 (1775 ± 92; N = 20) wide at ovarian isthmus; ovarian isthmus in posterior part of ovary ( Fig. 2E), 67–107 (86 ± 13; N = 20) long. Mehlis’ gland conspicuous ( Fig. 2E), posterior to ovarian isthmus, 174–227 (203 ± 14; N = 20) long, 267–334 (309 ± 20; N = 20) wide. Uterus medial ( Fig. 2E), saccate, ventral to vagina, extending from ovarian isthmus to posterior margin of cirrus sac, 685–822 (755 ± 38; N = 20) long, 617–788 (690 ± 49; N = 20) wide in mature and early gravid proglotids; uterine pore absent. Vitellarium follicular ( Fig. 2E); follicles 47–67 (55 ± 6; N = 26) long, 33–47 (37 ± 4; N = 26) wide, arranged in two lateral bands; vitelline bands extending throughout length of proglotid, partly or fully interrupted by terminal genitalia ( Fig. 2D), uninterrupted by ovary, 651–959 (820 ± 69; N = 20) wide on aporal side. Excretory vessels arranged in one dorsal and one ventral pair on each lateral margin of proglotid. Unembryonated, intrauterine eggs fusiform ( Fig. 2C), 114–145 (125 ± 9; N = 20) long, 20–27 (22 ± 2, N = 20) wide. Detached gravid proglotids not observed.

Remarks

Carrassoniella sinuosiceps ( Williams, 1959) comb. nov. is a poorly known species infecting the bluntnose sixgill shark, H. griseus . It was described by Williams (1959) based on specimens recovered from four shark individuals caught off the Irish coast. Te description by Williams (1959) provided detailed information on external and internal morphological features, including the musculature, nervous system, and male and female genitalia. In addition, the original description contained line drawings, including a detailed drawing of an entire specimen illustrating the segment progression ( Williams 1959: figs 1–6), and photomicrographs of histological sections. Te species was placed tentatively in the genus Phyllobothrium owing to similarities in scolex appearance to the type species, Phyllobothrium lactuca . However, Williams (1959) mentioned that given the incomplete descriptions of many species of Phyllobothrium at that time, including the ‘closely allied’ type species (sensu Williams 1959), the generic allocation was provisional and might change once more information on congeneric taxa became available. Carvajal (1974) reported Carrassoniella sinuosiceps (as Phyllobothrium sinuosiceps ) from the type host off the Chonos Archipelago ( Chile). Tis represented the first record of this species from the Pacific Ocean and the Southern Hemisphere. Carvajal (1974) claimed that owing to the lack of parasitological data on H. griseus , the parasite might have escaped detection and could potentially possess a much wider distribution. Henderson et al. (2003) recorded this species from H. griseus near the type locality off Ireland but did not provide detailed information on specimens. In his monograph on phyllobothriid tapeworms, Ruhnke (2011) re-examined the type specimen deposited in the NHM, London. Ruhnke (2011) revealed apparent morphological differences between Carrassoniella sinuosiceps (as Phyllobothrium sinuosiceps ) and the generic characteristics of Phyllobothrium , such as the uniloculate, foliose bothridia, euapolytic nature of the strobila, and absence of a vaginal sphincter, which made him question the generic placement. Terefore, Ruhnke (2011) considered Phyllobothrium sinuosiceps a species ‘ incertae sedis ’. Only recently, de Benedeto et al. (2023) collected six specimens of this species in the Mediterranean Sea off the Italian coast. Tese authors provided a brief description, a photomicrograph illustrating the terminal, mature proglotid, and the first scanning electron micrograph depicting the scolex of this species. Present specimens collected from the Balearic Sea add another geographical record from the western extension of the Mediterranean Sea. Carrassoniella sinuosiceps appears to be a dominant parasite of bluntnose sixgill shark populations in the eastern parts of the Temperate Northern Atlantic realm (sensu Spalding et al. 2007). However, this might be related to a higher ‘regional’ sampling effort of the shark host.

Carrassoniella sinuosiceps has been characterized by its large size, an almost spherical, uniloculate, highly foliose scolex not demarcated into distinct bothridia, presence of four weakly developed apical suckers, and a slightly craspedote strobila with proglotids containing a vast number of testes, a large cirrus sac, and absence of a uterine pore ( Williams 1959, 1968). Another species-specific characteristic is the armed cirrus that everts into the vagina, thereby ensuring self-fertilization of the same proglotid. Williams (1959) observed a membrane permanently covering the genital pore (see Williams 1959: fig. 11). Te enclosed genital opening prevents the cirrus from everting to the outside and instead forces it to extend into the vagina. Tere, the swollen basal part of the armed cirrus inserts into the permanently dilated distal part of the vagina. Although the presence of a membrane could not be confirmed in the present specimens, external labial structures were observed at the level of the genital pore. Tese external structures appear muscular and might act as a secondary mechanism to prevent the cirrus from exiting through the genital passage.

Table 1 provides comparative metrical data between the present specimen, type material and the specimen reported by De Benedeto et al. (2023) of Italy. Certain deviations were observed between the present specimens and the type series. Williams (1959) described Carrassoniella sinuosiceps (as Phyllobothrium sinuosiceps ) as an euapolytic species, with mature proglotids being shed and maturing in the intestinal tract of the chondrichthyan host. Te existing types deposited at the NHM in London consist of only two microscope slides, one containing the scolex, neck region, and immature strobila of the holotype and a second slide with a single, free gravid proglotid. Afer careful observation of the intestinal tract of H. griseus from Spanish waters, no gravid free proglotids were detected. In contrast, the largest specimen of Carrassoniella sinuosiceps contained many late mature and gravid proglotids. As such, the species is now considered apolytic rather than euapolytic. Williams (1959) also reported the species to possess between 700 and 800 testes arranged in three to four layers within mature proglotids. Te present specimens displayed a lower number of testes (i.e. slightly below 600) consistently arranged in three layers ( Table 1). Although a deviation of>100 testes in mature proglotids appears high at first glance, we believe that the testes numbers stated by Williams (1959) might represent an extrapolation in the absence of computerized technology aiding the enumeration process.

Conservation assessment of Carrassoniella sinuosiceps Carrassoniella sinuosiceps is a specialist parasite of the bluntnose sixgill shark ( H. griseus ). Tis shark host is a migratory species with a patchy, circumglobal distribution ( Ebert et al. 2021). With decreasing population trends, it is presently classified as Near Treatened (NT) in the International Union for the Conservation of Nature’s (IUCN) Red List based on assessment criteria A2bd ( Finucci et al. 2020). It is expected that the distribution of Carrassoniella sinuosiceps is significantly narrower than the one of H. griseus , which would ultimately warrant a classification in a higher threat level category. Yet, data (e.g. biogeographical distribution, infection parameters, and population trends) of this host-specific parasite are sparse, therefore limiting its threat predictability and assessment. A more cautious conservation assessment to assign a minimum conservation status for this parasite follows the conservation assessment methodology for animal parasites (CAMAP) introduced by Kwak et al. (2020). Based on criterion 6 (see Kwak et al. 2020), Carrassoniella sinuosiceps receives the same conservation status as its sole definitive host and is now classified as ‘Near Treatened’ until more data on the species becomes available and the species can be reassessed.