Classification

Phylum Platyhelminthes

Class Cestoda

Subclass Eucestoda

Order Cathetocephalidea

Order Diphyllidea

Order Lecanicephalidea

Order Litobothriidea

Order Phyllobothriidea

Order Rhinebothriidea

Order “Tetraphyllidea”

Cathetocephalidea Schmidt and Beveridge, 1990 (Order)

Introduction

Species in the order Cathetocephalidea Schmidt and Beveridge, 1990 are segmented worms and are parasites of the spiral intestine (also called the spiral valve) of sharks. Despite their low species richness, they have an almost cosmopolitan distribution. Cathetocephalidea is one of the 19 orders constituting the class Cestoda (Platyhelminthes). Their name is derived from the Greek terms kathetos (= perpendicular) and kephalē (= head), which refers the position of the fleshy fixation organ (scolex) with respect to the body (strobila).

This order was proposed by Schmidt and Beveridge (1990) based on the uniqueness of the scolex of the 2 species known of the family Cathetocephalidae Dailey and Overstreet, 1973 although the strobila and proglottids are similar to those in the orders Tetraphyllidea, Trypanorhyncha, and Lecanicephalidea. However, Euzet (1994) maintained it at the family level and included in the Tetraphyllidea. Currently, the validity of the order was verified using molecular data (Caira et al., 2005).

This order contains the families Cathetocephalidae and Disculicepitidae. Cathetocephalidae comprises the genera Cathetocephalus (with 3 species) and Sanguilevator (with 1 species). The genus Disculiceps (with 2 species) is included in Disculicepitidae. In addition, 5 taxa are descriptions (nomina nuda = nude names), meaning that a species name was published without the designation of type specimens nor were sufficient data given for valid descriptions (Caira et al., 2017a).

Main Morphological Characteristics

The body of individuals within the order Cathetocephalidea Schmidt and Beveridge, 1990 are polyzoic (that is, the strobila is composed of more than 1 proglottid) and are of moderate size, 23 mm-long in Sanguilevator yearsleyi and up to 134 mm-long in Cathetocephalus resendezi, according Caira and colleagues (2005). The scolex is fleshy and simple (meaning, lacking suckers, bothridia, or armature), is perpendicular to the axis of the strobila, and is T-shaped (except in species of Disculiceps spp., in which it is round in cross section). The scolex is divided into 2 regions: An apex that is cushioned with a rugose base (and which is referred to as a collar in species of Disculiceps). The anterior region of the scolex in Cathetocephalus and Sanguilevator possesses bands of minute papillae in the middle portion, but which are absent in Disculiceps (Nock and Caira, 1988). A distinctive trait of the scolex of Sanguilevator is the presence of 3 dorsoventral pairs of spherical chambers and 2 pairs of elongate transverse channels (1 dorsal and 1 ventral, with numerous lateral posterior branches) located in the center of the scolex proper (Caira et al., 2005; 2017a).

The strobila may be fixed to the scolex in any position of the bottom surface of the rugose base. It is acraspedote, that is, without velum (see Palm, 2004), except in Cathetocephalus australis whose proglottids have velum, that is, they are slightly craspedote (Dailey and Overstreet, 1973; Schmidt and Beveridge, 1990; Euzet, 1994; Caira et al., 2005; 2017a). Most of the species are euapolytic, meaning that there is detachment of the mature proglottids when the eggs are infective (Khalil et al., 1994) or anapolytic, meaning that proglottids remain on the strobila until they senesce and eventually degenerate (Caira et al., 2016), although anapolysis is only observed in both species of Disculiceps (Nock and Caira, 1988). The mature proglottids are longer than they are wider in Cathethocephalus and Sanguilevator and are almost square-shaped in Disculiceps (Caira et al., 2017a).

Specimens within the order Cathetocephalidea Schmidt and Beveridge, 1990 are hermaphroditic, with numerous testes, varying from 77 (in Sanguilevator yearleyi) to 500 (in Cathetocephalus thatcheri). The cirrus sac is bent anteriorly and the cirrus is armed. The genital pore alternates irregularly, and is marginal, except in Disculiceps, and is equatorial, except in Cathetocephalus (where it is post-equatorial). The ovary is bi-lobed and the vagina opens anterior to the cirrus sac at the genital atrium. The uterus is medial and is weakly branched, becoming sacciform in some species. In both species of Disculiceps, the uterus opens by longitudinal dehiscence (Nock and Caira, 1988). The vitelline follicles are circum-medullary in cross section. The eggs are clustered in cocoons (Nock and Caira, 1988; Schmidt and Beveridge, 1990; Caira et al., 2005).

Description and Summary of a Representative Species

Note: This work is not intended for the purposes of zoological nomenclature.

Cathetocephalus resendezi Caira et al., 2005

The worms are relatively large (29–134 mm-long) with 79–340 proglottids, and they are acraspedote and euapolytic. The body is covered by michrotriches (tegumentary projections with an apical electro-dense portion, following Chervy, 2009). The morphology of the scolex is described for the order, with the rugose base inconspicuous, covered by palmate microthrix. There is a papillate band with a folded base. The papillae are relatively short throughout the anterior one-half to two-thirds. Mature proglottids are longer than they are wider, bearing 128–285 testes arranged in a single layer. The cirrus sac is bent anteriorly, with bladelike spinitriches (which are a type of microthrix with > 200 nm in basal width; see Chervy, 2009). The genital pore is post-equatorial. The ovary is H-shaped in the ventral view. The vagina opens anterior to the cirrus sac at the genital atrium. The uterus is slightly sinusoidal. The vitellaria are follicular and distributed along the entire proglottid (see Caira et al., 2005).

Taxonomic summary

Type host: Bull shark, Carcharhinus leucas.

Site of infection: Spiral intestine.

Type locality: Bahía de Los Ángeles (28° 85′ 50″ N, 113° 83′ 20″ W), Baja California, Gulf of California, Mexico.

Type specimens are listed here and additional details can be found in the original paper where this species was described (Caira et al., 2005): Holotype (CNHE 5300); paratypes (CNHE 5301; USNM 96411; LRP 3717–3722).

Order Cathetocephalidea Schmidt and Beveridge, 1990 in Relation to Each Other

To date, 3 valid species are recognized in the genus Cathetocephalus: Cat. thatcheri, parasitizing the bull shark Carcharinus leucas from the Gulf of Mexico, United States (Dailey and Overstreet, 1973), Cat. australis, parasitizing the copper shark Car. brachyurus from Goolwa, South Australia (Schmidt and Beveridge, 1990), and Cat. resendezi, found in the spiral intestine of the bull shark Car. leucas collected in the Gulf of California, Mexico (Caira et al., 2005). The morphological differentiation among the 3 species of the genus is mainly based on features of the scolex: In Cat. thatcheri the papillae are slender and elongate, arranged in the distal third of the papillar band (versus the short, thick, and irregular papillae in Cat. resendezi, distributed from the distal one-half to two-thirds of the band). In the third species, Cat. australis, the papillae are disposed in 2 bands separated by a medial smooth band. In addition, the configuration of the rugose base of the scolex follows a gradient-like pattern, ranging from inconspicuous in Cat. resendezi, to slightly rugose in Cat. thatcheri, and conspicuous in Cat. australis.

Another distinctive feature is the presence of lobulated margins of the ovary of Cathetocephalus resendezi, which is unlike the other 2 species, in which continuous margins are evident (Dailey and Overstreet, 1973; Schmidt and Beveridge, 1990; Caira et al., 2005).

Despite the lack of bothridia and the presence of bands of papillae on its scolex, Cathetocephalidae was placed in the order Tetraphyllidea. However, Schmidt and Beveridge (1990) considered that these characteristics warranted the establishment of a new order for this family. Fifteen years later, Cathetocephalidea was the first order formally recognized since the disintegration of Tetraphyllidea, based on molecular evidence using the gene fragments 18S and 28S (Caira et al., 2005). Other closely related groups that derive from Tetraphyllidea are Phyllobothriidea and Onchoproteocephalidea, these being the sister taxa of Cathetocephalidea (Waeschenbach and Littlewood, 2017). Unlike Cathetocephalidea, specimens from both of those other orders have suckers, bothridia, or armature. In the phylogenetic analysis of Caira and colleagues (2014b), Cathetocephalidea is closely grouped among the acetabulate orders of cestodes. Based on these results, the authors suggest the derived condition of the non-acetabulate scolex.

Life Cycles

To date, the life cycle of members of this order remains unknown. Notwithstanding, members of this group show a high affinity to Carcharhiniformes sharks, particularly Carcharhinidae and Sphyrnidae. This host-parasite association seems to suggest the oioxenous (that is, a 1:1 relationship between parasite and host species) nature of these cestodes. According to the original description of the 6 species known for this order, their distribution is almost worldwide. However, Caira and colleagues (2017a) pointed out that they have not been recorded from the Arctic and Southern Ocean marine realms as established by Spalding and colleagues (2007).

Unique Features of the Order Cathetocephalidea Schmidt and Beveridge, 1990

The multistrobilization (that is, the formation of multiple strobilae attached to a single scolex) observed by Dailey and Overstreet (1973) in Cathetocephalus thatcheri (occasionally with 14 to 24 strobilae per individual) seems to be an exclusive character of this species more than a general feature at the order level, since it has not been found in other members of this group and only reported in 1% of the specimens collected by Dailey and Overstreet (1973). According to these authors, a more detailed examination of this phenomenon must be conducted to determine if it represents a type of asexual multiplication or an abnormal condition of the specimens studied by them.

The accumulation of blood cells in the chambers and channels of the Sanguilevator yearsleyi escolex is a feature that distinguishes it within the Cathetocephalidea and the cestodes in general. According to Caira and colleagues (2005), there is no plausible explanation for how the cestodes separate the host’s cells as well as what the purpose of this accumulation may be.

Diphyllidea van Beneden in Carus, 1863 (Order)

Introduction

This group of small and polyzoic cestodes inhabiting the spiral valve of elasmobranchs (most commonly, species of Carcharhiniformes, Myliobatiformes, Rajiformes, and Rhinopristiformes, according to Ivanov and Caira, 2013) is distributed worldwide. One of the most remarkable traits of this group is the presence of only 2 bothridia on the scolex (feature from which the name of this order derived: di (= 2, Latin) and from phyllidium (= leaf, Greek)) and a genital pore at the midventral region. Despite the wide variation in the presence or absence and arrangement of the scolex structures, in general diphyllideans may bear an apical organ armed with hooks, lateral hooklets, a cephalic peduncle that may be armed with spines, and a corona of spines (Caira et al., 2013; 2017d).

This order, proposed by van Beneden in Carus (1863), currently is widely accepted, although their validity has been controversial (see Caira et al., 2017d). The monophyly of the order has been demonstrated by morphological data by Ivanov and Hoberg (1999) and ratified based on molecular data by Caira and colleagues (1999; 2013) and Waeschenbach and colleagues (2012).

This order contains only 1 family (Echinobothriidae) with 6 genera and 59 described species. Echinobothrium is the genus with the highest number of species (see Figure 1), with 33, followed by Halysioncum, with 16 species, Coronocestus, with 6 species, and Ditrachybothrium, with 2 species. The genera Andocadoncum and Ahamulina are monotypic (Caira et al., 2017d).

Diphyllideans are cosmopolitan. According to Spalding and colleagues (2007), its members have been recorded in all marine realms.

Main Morphological Characteristics

Diphyllideans are polyzoic worms, relatively small in body size, ranging from 0.46 mm in Echinobothrium weipaense (Ivanov and Caira, 2012) to 95.3 mm-long in the largest species (Ditrachybothridium piliformis, see Faliex et al., 2000).

The scolex is composed of a pair of sessile bothridia (1 dorsal and 1 ventral), often bearing a corona of spines, a cephalic peduncle armed with spines, and hooks and lateral hooklets on the apical organ (Khalil, 1994; Caira et al., 2017d). In contrast, the cephalic peduncle in Ditrachybothridium is short and unarmed and lacks apical hooks (Ivanov and Hoberg, 1999). The scolex is covered by spinitriches of different types, distributed in patterns that vary at the species level. The cephalic peduncle lacks spinitriches and filitriches are present in some species (Ivanov and Caira, 2013).

They have acraspedote and apolytic strobila (that is, those that release gravid proglottids). Their mature proglottids are longer than they are wider. A common trait among the species of this order is the arrangement of the hermaphroditic reproductive system with the genital pore placed on the mid-ventral line in the posterior part of the proglottid, a bi-lobed ovary in cross section located in the posterior margin, as well as an absence of uterine pores (Ivanov and Hoberg, 1999). Other reproductive characteristics shared by diphyllideans are the presence of a vaginal opening posterior to that of the unipartite cirrus sac, a cirrus with spinitriches, testes disposed in 2 columns anterior to the ovary (between 4–6 in Halysioncum rayallemangi, according to Tyler (2006) to 43–81 in Ditrachybothridium piliformis; see Faliex et al. (2000)), vitellaria in 2 lateral bands or circumcortical in cross section, and a saccular uterus (Caira et al., 2017d). Eggs in most species are without filaments, and some have a polar projection, such as Echinobothrium harfordi, and some have a polar filament, such as Echinobothrium affine (Ivanov and Hoberg, 1999; Tyler, 2006).

Figure 1. Line drawings. A, D–H) Echinobothrium nataliae. A) Whole worm; D) scolex; E) L lateral hooklets; F) egg. G) mature proglottid; H) detail of terminal genitalia, lateral view; B) Echinobothrium reginae, whole worm; C, I) Echinobothrium vojtai; C) whole worm; I) egg. Abbreviations: A1) First A (anterior) hook; B1) first B (posterior) hook; cs) cirrus sac; gp) genital pore; isv) internal seminal vesicle; LH) lateral hooklets; ov) ovary; ut) uterus; va) vagina; vf) vitelline follicles.
(Source: Kuchta and Caira, 2010. License: CC BY.)

Description and Summary of a Representative Species

Note: This is not intended for the purposes of zoological nomenclature.

Halysioncum mexicanum (Tyler & Caira, 1999) Caira et al., 2013

These are short-bodied worms (1.16–0.27 mm length), consisting of 4–10 segments, and are longer than they are wide as they reach maturity. Generally, the last segment is the widest portion of the body (0.11–0.44 mm). The scolex is constituted of 2 large oval bothridia (1 ventral and 1 dorsal) and an apical rostellum armed with 2 groups of 23 large apical hooks, 1 dorsal and 1 ventral. The hooks are flanked by 1 continuous row of 10–13 small lateral hooklets on each side. The surface of the bothridia is covered with palmate microtriches, with the number of digits varying along bothridia (3 or 4 at the anterior-most proximal area and 6 at the posterior region). They include short filiform microtriches spread along the proximal surfaces. The microtriches change from palmate to slender filiform abruptly, limiting the border between the distal and proximal surfaces of the bothridia. The cephalic peduncle is large and wide at the middle point, armed with 8 longitudinal columns of 23–40 spines with a triradiate base. The base length decreases from the anterior to the posterior region of the cephalic peduncle, which is covered by short filiform microtriches. The strobila is acraspedote, formed by 1–3 mature segments and 1 gravid proglottid. The testes (10–20 in number) are arranged in 2 or 3 columns at the anterior half of each segment. The cirrus sac is expanded, and is armed along its length with robust curved spines. The ovary is bi-lobed and H-shaped. The ovarian isthmus is stout. Mehlis’ gland is prominent. The vagina is robust, ventral, and positioned immediately adjacent to the genital atrium. The genital pore is situated mid-ventrally. The uterus is dorsal, extending from the ovarian isthmus to the anterior margin of a gravid segment. A uterine pore is absent. The follicular vitellaria are arranged in 2 wide lateral bands uninterrupted along the proglottid, and are joined posterior to the ovary. There are small filamented eggs. The excretory ducts are lateral.

Taxonomic summary

Type host: Snouted eagle ray, Myliobatis longirostris.

Site of infection: Spiral intestine.

Type locality: Bahía de Los Ángeles, Gulf of California, Mexico (28º 55′ N, 110º 25′ W).

Type specimens are listed here and additional details can be found in the original paper where this species was described: Holotype (CNHE 3343); paratypes (CNHE 3344–3345; USNPC 88220–88221; HWML 39912–39914).

Members of the Order Diphyllidea van Beneden in Carus, 1863 in Relation to Each Other

Of the 15 additional species described for the genus Halysioncum, H. mexicanum has 23 apical hooks on its scolex. Therefore, H. mexicanum can be distinguished from 6 of the other species because these have a smaller number of hooks: H. fautleyae (11 hooks), H. pigmentatum (20 hooks), H. bonasum (11 hooks), H. hoffmanorum (19–21 hooks), H. californiense (21 hooks), and H. kishiense (10–11 hooks), and from an additional 6 species because they have a greater number of hooks (between 25 and 29): H. nataliae (27–29 hooks), H. reginae (29 hooks), H. vojtai (29 hooks), H. euzeti (25 hooks), H. megacanthum (27 hooks), and H. gibsoni (27 hooks). Finally, the number of apical hooks on the scolex of H. mexicanum is similar to that of H. raschii (23–25 hooks) and identical to the number of hooks contained within H. arafuerense and H. rayallemangi. However, the length of the strobilus in H. raschii is considerably greater (8.6–21.5 mm) than that of H. mexicanum (1.16–5.27 mm) and the number of digits in the microtriches of H. raschii can be up to 15 while in the Mexican species its number ranges from 3–6. The number of spines of the cephalic peduncle is another trait that makes it possible to differentiate H. arafuerense and H. rayallemangi from H. mexicanum, since this number ranges from 20 to 24, 2 to 5 and 23 to 40, respectively. Additionally, the number of testes of H. rayallemangi is considerably lower (4–6) than that of H. mexicanum (10–20) (see Tyler, 2006; Kuchta and Caira, 2010; Ivanov and Caira, 2013; Moghadam and Haseli, 2014).

In the first phylogenetic study about the intrageneric relationships of Diphyllidea, based on morphological traits, Ivanov and Hoberg (1999) recognized monophyly of the order. However, the results suggested that 2 of the 3 formerly recognized genera (Macrobothridium and Echinobothrium) could be considered synonyms, validating the independence of Ditrachibothridium, a proposal ratified by Tyler (2006). The molecular confirmation of this hypothesis was made by Caira and colleagues (2013), who also erected 2 new genera (Halysioncum and Coronocestus) based on species previously included in Echinobothrium. In the same work, the authors identified a new genus of parasite provisionally termed Leucoraja, which was formally described a year later and named Andocandoncum (Abbott and Caira, 2014).

Life Cycle

The complete life cycle of species of Diphyllidea is poorly known (Tyler, 2001; Bray and Olson, 2004). According to Caira and Reyda (2005) the diphyllidean cestodes follow the same pattern of life cycles as other elasmobranch cestodes. In this pattern the life cycle appears to involve 2 intermediate hosts and 1 elasmobranch as the definitive host. The intermediate hosts are species of Mollusca, Arthopoda, and Actinopterygii. There are many records of larvae in teleost fishes and invertebrates such as crustaceans and molluscs (Bray and Olson, 2004). For example, Cake (1976) reports larvae from 1 species of Echinobothrium from the gastropod Cantharus cancellaerius and Narrasius vibex from the northern Gulf of Mexico; Jones and Beveridge (2001) collected a single plerocercoid of Echinobothrium chisholmae from the decapod Penaeus longistylus from Heron Island, Queensland, Australia, and Muñoz and colleagues (2001) found larvae in the intestine of the fish Notothenia c.f. angustata in the Gulf of Arauco, Chile. The adults of this order parasitize mainly batoids (skates and stingrays) (Tyler, 2001) although some species of Coronocestus have been recorded in sharks of the genera Mustelus and Iago (Ivanov, 1997; Haseli and Azad, 2015). Finally, Tyler (2006) suggests that diphyllidean species follow this pattern of life cycle: Eggs are shed with the feces of the definitive host, and posteriorly ingested by a first intermediate host (an invertebrate) such as an amphipod. In the intestine, the eggs hatch, releasing a hexacanth larva which then develops a procercoid. Then, the amphipod is ingested by the second intermediate host (a crab or a shrimp). Into this host the procercoid encysts in the liver and develops a plerocercoid. Finally, this stage is eaten by a definitive host (a shark or batoid) in which the cestodes reach sexual maturity. In some cases, the plerocercoid can be ingested by another type of host (a teleost fish), acting as a paratenic host (which is an organism that carries the immature stage of parasites).

Additional Notes about the Morphology

Diphyllidea and Trypanorhyncha are the only 2 orders of parasites of elasmobranchs in which metacestodes harbored by the last intermediate host bear the diagnostic taxonomic characters of the adult scolex (Beveridge et al., 2017; Caira et al., 2017d). This allows identification of the metacestodes to the species level using morphology only.

The morphology of the scolex in Diphyllidea shows a wide range of modification in terms of the presence or absence and arrangement of structures. These variations oscillate from the total absence of spines in the cephalic peduncle and hooks in the scolex-proper of Ditrachibothridium (Faliex et al., 2000), to the lack of spines on the cephalic peduncle in some species of Echinobothrium and Ahamulina (Tyler, 2006; Marques et al., 2012), or may have between 100 and 107 spines along each of 8 longitudinal rows disposed in the cephalic peduncle, as is found in Halysioncum euzeti (Campbell and Carvajal, 1980).

Lecanicephalidea Hyman, 1951 (Order)

Introduction

Lecanicephalidea (the name derived from Greek, lekane = dish or pot and kephalē = head) is an order of cestodes remarkably diverse in its morphology. They are mainly parasites of the spiral intestine of batoid elasmobranchs distributed  around the world (Jensen et al., 2016). The main diagnostic trait of this group is the presence of an apical structure  on the scolex, called a myzorhynchus or, more recently, termed the apical organ, which is found in a wide variety of forms. Other important characteristics of this group include: The presence of 4 suckers (also termed bothridia), proglottids with the vagina opening posterior from the cirrus sac into the genital atrium (Jensen et al., 2017), and a sizeable vas deferens often expanded into a sacciform external seminal vesicle that extends from the level of the ovarian isthmus to the cirrus sac (Jensen et al., 2016).

They were discovered in the 1890s. The first valid species described for this order was Polypocephalus radiatus Braun, 1897; however, the ordinal status of Lecanicephalidea has been questioned (their elevation to this level was even invalidated by Butler (1987)) and its species were often included in the order Tetraphyllidea (Jensen et al., 2017). Currently, based on molecular data analyses, Lecanicephalidea is considered the earliest diverging lineage among the acetabluate cestode orders (Jensen et al., 2017).

According to Jensen and colleagues (2017), Lecanicephalidea contains 8 families with 29 genera and 90 described species, as well as 7 incertae sedis species and 66 species inquirendae. Polypocephalus is the genus with the highest number of species (16 species; see Figure 2), while Adelobothrium, Cephalobothrium, Collicocephalus, Rexapex, Anthemobothrium, Corrugatocephalum, and Quadcuspibothrium are monotypic.

Main Morphological Characteristics

The strobila of this group of polyzoic cestodes is relatively small since the smallest worm measures less than 500 mm (Jensen, 2005) and only a few species have strobila measuring up to 6 cm, according to Butler (1987). Lecanicephalideans are generally euapolytic, but some species can be anapolytic, apolytic, and hyperapolytic. The proglottids tend to be craspedote (or may rarely be acraspedote) and may be laciniated (fringed in the posterior end) or not (Jensen et al., 2016).

Figure 2. Scolex and proglottids of Polypocephalus moretonensis Butler, 1987, holotype specimen from the Queensland Museum, South Brisbane, Queensland, Australia. See the item at this link from the Queensland Museum for more information about this specimen.
(Source: Queensland Museum, 2023. License: CC BY.)

With the exception of Aberrapex and Paraberrapex, which lack an apical structure in the scolex, the remaining lecanicephalideans are distinguished from most other orders of cestode parasites of elasmobranchs by having this structure (Jensen, 2005). The apical organ can be external or entirely internal; its morphology varies from a foldable sheet to an oval muscular pad or may present as an inverted cone with papilliform projections. In families such as Cephalobothriidae, there can be a glandular sphere. In others, such as Polypocephalidae, the apical organ is divided into tentacles. The tentacles can be retractable (or not) and some are invaginable. The scolex is also characterized by having 4 uniloculate acetabula or bothridia (and are biloculate only in Zanobatocestidae and diamond-shaped only in Quadcuspibothrium). Immature proglottids may be laterally expanded or not, and may form a trough (although only in Eniochobothriidae) (Jensen et al., 2016).

Reproductive Structures

Lecanicephalideans are hermaphroditic.

The female reproductive system is markedly heterogeneous; it consists of the following structures. It contains an ovary that is variable in form (it may be H-shaped, bi-lobed, tetra-lobed in cross section, digitiform, irregularly lobed with each lobe divided in 3 sub-lobes, etc.). It includes a vagina, which may be positioned medially, laterally, or sub-laterally (or may even be absent), opening into a genital atrium posterior to the cirrus sac. It includes a follicular vitellarium, generally arranged in 2 lateral bands. The vitellarium may reach the posterior end of the proglottids or only the anterior border of the ovary, and they do not exceed the anterior limit of the testicular field. The vitellarium may be distributed in 3 fields (1 posterior to the ovary, 1 between the genital atrium and the anterior margin of the ovary, and a field consisting of 2 lateral bands before the cirrus sac) or may present in 2 lateral bands from the middle of the cirrus sac to the level of the ovarian isthmus. It includes a uterus that is medial, saccate, or bisaccate (and constricted to the level of the genital atrium), and is variable in extent, from the anterior of the ovary to the genital pore, or almost occupying the entire length of the proglottid (Jensen, 2005; Jensen et al., 2016).

In contrast, the morphology of the male reproductive system is more homogeneous: The number of testes varies from 4 (in Seusapex karybares) to more than 40 (in Tetragonocephalus kazemii) that are distributed commonly in 1 to 2 columns, located anteriorly to the genital pore, ovary, or cirrus sac (Russell and Jensen, 2014; Jensen et al., 2016; Roohi and Malek, 2017). Internal and external seminal vesicles may be present or absent. The cirrus sac is pyriform (or elliptical in some Polycephalidae). The cirrus is unarmed (although it is armed in Tetragonocephalidae and Eniochobothriidae and rarely in Polycephalidae and Lecanicephalidae). The genital pore is lateral (or sub-lateral in Polycephalidae), alternating irregularly (Jensen, 2005; Jensen et al., 2016).

Description and Summary of a Representative Species

Note: This work is not intended for the purposes of zoological nomenclature.

Aberrapex senticosum Jensen, 2001

These are small, euapolytic worms, 1.48–6.33 mm-long, with a maximum width of 31–38 mm at the ends of the strobila. The scolex consists of 4 bothridiated acetabula. There is apical modification of the scolex proper and an apical organ is absent. The acetabula and scolex proper are partially covered with large blade-like spiniform microtriches and long filiform microtriches. A cephalic peduncle is absent. The strobila has long filiform microtriches, becoming wider toward the posterior margins of the proglottids. The proglottids are craspedote and laciniate. There are 29–36 immature proglottids with 1 or 2 proglottids containing 20–40 testes arranged in a single field from the anterior margin of the proglottid to the anterior limit of the ovarian isthmus. The external seminal vesicle is wide and saccate, while an internal seminal vesicle is absent. The cirrus sac is pyriform and the cirrus is unarmed. The ovary is H-shaped in the dorsoventral view and tetra-lobed in cross section. It is also lobulated and symmetrical. The vagina runs laterally from the ootype zone to the genital pore; it is open posterior to the cirrus sac into the genital atrium. The genital pore is lateral, pre-equatorial, and alternates irregularly. The uterus is saccate, extending along the midline of the proglottid, almost reaching the anterior margin of the proglottid. A uterine pore is absent. The vitellaria are follicular, medullar, and lateral. The follicles are distributed along the entire length of the proglottid, only interrupted by the ovary (Jensen, 2001).

Taxonomic summary

Type host: Bat eagle ray Myliobatis californica Gill, 1865 (Rajiformes, Myliobatidae).

Type locality: Santa Rosalía (27° 81′ 99″ N, 112° 81′ 79″ W), Baja California, Mexico.

Site of infection: Spiral intestine.

Type specimens are listed here and additional details can be found in the original paper where this species was described: Holotype (CNHE 4188) and 2 paratypes (CNHE 4189); 3 paratypes (USNPC 91208); 2 paratypes (HWML 16374); 7 paratypes (LRP 2152–2158).

Lecanicephalidea Hyman, 1951 Taxonomy

In addition to Aberrapex senticosum, 6 more species of the genus parasitizing myliobatiform batoids from tropical and temperate waters have been described to date: A. arrhynchum (Brooks et al., 1981) Jensen, 2001; A. ludmilae Menoret, Mutti & Ivanov, 2017; A. manjajiae Jensen, 2006; A. sanmartini Menoret et al., 2017; A. vitalemuttiorum Menoret, Mutti & Ivanov, 2017; and A. weipaensis Koch et al., 2012 (Menoret et al., 2017). Aberrapex senticosus can be distinguished from the other species included in the genus since it has the highest number of testes (20–40 versus 18–25, 24–31, 10–19, 11–16, 15–21, and 10–17, respectively). In addition, A. ludmilae and A. arrhynchum lack an external seminal vesicle (while it is present in A. senticosum). In the remaining species, hastate spinitriches are entirely absent in the acetabular surface (A. weipaensis), restricted to the central region of the acetabula (A. manjiajae) or cover only two-thirds of the distal acetabular surface (A. sanmartini and A. vitalemuttiorum) while in A. senticosus hastate spinitriches cover the entire distal acetabular surface (Jensen, 2001; 2006; Koch et al., 2012; Menoret et al., 2017).

The first phylogenetic studies on lecanicephalids were based on morphological data (Caira et al., 1999; 2001; Jensen, 2005). In such studies, this group of cestodes was generally nested as a clade by the presence of an apical structure in the adult stage. When authors such as Jensen (2005) included some species lacking apical structure, they were positioned as the first divergent lineages of the order. Relative to its relationship with other orders of cestodes, Caira and colleagues (1999; 2001) detected possible affinities with cyclophyllideans.

Almost simultaneously, several works based on molecular evidence established Lecanicephalidea as the earliest lineage among the acetabulate cestode orders (Olson and Caira 1999; Olson et al., 2001; Caira et al., 2005; Waeschenbach et al., 2007).

The most recent and comprehensive analyses on the relationship among lecanicephalidean cestodes was conducted by Jensen and colleagues (2016); these authors confirmed the monophyletic nature of the order and recognized 8 major groups as independent families: 4 previously existing (Lecanicephalidae, Polypocephalidae, Tetragonocephalidae, and Cephalobothriidae) and 4 new families (Aberrapecidae, Eniochobothriidae, Paraberrapecidae, and Zanobatocestidae).

Life Cycles

Life cycles of cestodes of the order Lecanicephalidea are poorly known; however, according to Caira and Reyda (2005) larvae of these cestodes have been registered in some groups of invertebrates, mainly bivalves (molluscs) and crustaceans, as well as in few actinopterygians. Based on the scarce available information on the developmental stages of lecanicephalideans, Caira and Reyda (2005) suggested that they lack a coracidium (that is, a hexacanth embryo is inside the egg); plerocerci have been found in bivalves and gastropod molluscs and plerocercus, their terminal larval stage, in actinopterygians such as Scomberoides commersonnianus from the Arabian Gulf (Bannai et al., 2014).

Lecanicephalideans have circumglobal distribution; currently, members of this cestode order have been described from 8 of the 12 marine biogeographic realms, with the greatest concentration of species (69%) recorded in the central Indo-Pacific (Jensen et al., 2017).

Additional Notes about the Morphology

As noted above, Lecanicephalidea is an order of cestodes remarkably diverse in its morphology. For example, many lecanicephalideans possess additional features of proglottid anatomy that are unusual for other cestodes hosted by elasmobranchs (Jensen et al., 2017). For example, the genus Hexacanalis was erected by Perrenoud (1931) based on the presence of 6 excretory vessels, while the most common condition in the cestodes is the presence of 2 dorsal and 2 ventral excretory vessels. Jensen and colleagues (2016) pointed out that the different number of pairs of excretory vessels (1, 3, or more) is so particular, that it can be considered a diagnostic trait of the family Lecanicephalidae. In the same way, 1 species included in this genus (Hexacanalis folifer) is unique among lecanicephalideans by having a U-shaped ovary in cross section and proglottids with prominent posterior dorsoventral processes in the form of large lappets (Cielocha and Jensen, 2011).

On the other hand, despite the scarce knowledge about the gravid proglottids of the members of this order, it has been determined that the morphology of the eggs shows drastic variations, even among the congeneric species: In Anteropora comica, the eggs are covered with numerous small, regularly-spaced surface protuberances without polar filaments, while in A. klosmamorphis, the eggs have a corrugated surface and bipolar filaments (Jensen et al., 2011). Something similar occurs with the cocoons, since in some species (for example, Zanobatocestus major), cocoons contain only 2 eggs while in others (such as Z. minor), these are arranged in cocoons with hundreds of eggs (Jensen et al., 2014).

Litobothriidea Dailey, 1969 (Order)

Introduction

The order Litobothriidea was established by Dailey (1969) to accommodate 2 new species recovered from the bigeye thresher shark Alopias superciliosus, from the California coast. This proposal was based on the unique holdfast features; according to Dailey (1969), the scolex consists of an apical sucker with an auxiliary holdfast modification of the anterior segments of the strobila. The name Litobothriidea, derived from the Greek word lito (= simple) and bothros (= trench), reflects the simplicity of the scolex. Caira and colleagues (1999) pointed out that the region posterior to the apical sucker can be constituted of up to 5 pseudosegments, a subset of which is cruciform in cross section.

Considering the 9 orders of cestodes parasitizing elasmobranchs, Litobothriidea is the second-least speciose group after Cathetocephalidea (constituting 6 species) (Caira et al., 2017b). The 9 species included in the order, all belonging to the genus Litobothrium, infect the spiral intestine of Lamniformes sharks from Mexico and Taiwan (Caira et al., 2017a) in the tropical eastern Pacific to the central Indo-Pacific marine ecoregions, according to Spalding and colleagues (2007).

Main Morphological Characteristics

They are medium-sized worms with a body length ranging from 1.65 mm (as in Litobothrium alopias) to 32.8 mm (as in L. aenigmaticum). The scolex comprises a single and well-developed apical sucker and 3–5 cruciform pseudosegments (but which is dome-shaped in L. aenigmaticum with an extensive cephalic peduncle and special tissue composition). Bothridia and a neck are absent. They have dorsoventrally flattened strobila with numerous craspedote proglottids (13–88 in number) that may be laciniated or not. They are apolytic, anapolytic, euapolytic, or extremely hyperapolytic (the latter a feature only of L. aenigmaticum). They are hermaphroditic with a single set of reproductive organs by segment, medullary located. The genital pores are lateral and alternate irregularly. The cirrus sac is pyriform, and the cirrus may be armed or not. There are numerous testes (15–84) that are medullary and preovarian, in general, arranged in 2 columns. They extend from the anterior end of the proglottid to the anterior margin of the ovary, rarely overpassing it. The vagina opens into the genital atrium anterior to or at the level of the cirrus sac. The ovary is usually an inverted U-shape and is medial and posterior. The vitellaria are follicular, encircling a medullary parenchyma, with the exception of L. amsichensis, in which it is circumcortical. The uterus commonly reaches the posterior margin of the cirrus sac and is armed at the base in L. amsichensis. The eggs do not reach the oncosphere stage while in the uterus (Dailey, 1969; 1971; Kurochkin and Slankis, 1973; Caira and Runkle, 1993; Olson and Caira, 2001; Caira et al., 2014). The structure of the reproductive organs of L. aenigmaticum remain unknown because mature and gravid proglottids have not been found in specimens from that group (Caira et al., 2014a).

Description and Summary of a Representative Species

Note: This work is not intended for the purposes of zoological nomenclature.

Litobothrium amplificum (Kurochkin and Slankis, 1973) Euzet, 1994

These are cestodes with a short body (3.3–6.8 mm). The scolex consists of a cup-shaped apical and muscular sucker and 4 cruciform pseudosegments. The first pseudosegment has inconspicuous dorsomedial and ventromedial projections; pseudosegments 2 and 3 have well-developed projections, and in the last pseudosegment, the projections are highly modified. The lateral margins are divided into 3 projections: 1 small central, 1 large dorsal, and 1 large ventral, and the last 2 are recurved medially. The first 2 pseudosegments are armed with a single row of spine-like structures that are embedded in its posterior margins.

The first 3 segments of the strobila are highly laciniated, with the laciniations of the first reaching the posterior end of the third segment. The body is covered with filitriches, which are longer in reproductive segments than those in the immature proglottids.

The strobila is euapolytic and consists of 13–19 craspedote segments, 12–19 immature segments that gradually become longer than they are wide and with 0–2 mature segments that are longer than they are wide. There are 53–84 oval to round testes. The cirrus sac is pyriform and extends approximately to the median line of the segment. The cirrus is highly coiled and is armed with spiniform microtriches. The vas deferens is anterior to the cirrus sac and is bifurcated prior to the ovary. The ovary is inverted, U-shaped, posterior, and bi-lobed in cross section.

The genital pore is located at 60–78% of the segment length from the posterior end and alternates irregularly. Mehlis’ gland is posterior to the ovary in the segment. The uterus extends from the ovarian isthmus to the posterior margin of the cirrus sac. The vitellarium is follicular and is positioned across the length of the segment, interrupted by the ovary and cirrus sac.

Taxonomic summary

Host: Pelagic thresher shark Alopias pelagicus Nakamura, 1935.

Site of infection: Spiral intestine.

Type locality: Gulf of Tehuantepec, Oaxaca, Mexico. Additional localities: Bahía de los Ángeles (28° 55′ N, 113° 32′ W) and Santa Rosalía (27° 19′ N, 112° 17′ W), Gulf of California, Mexico.

Type specimens: Unknown.

This species was described by Kurochkin and Slankis (1973) as Renyxa amplifica from 2 specimens of Alopias superciliosus from the Gulf of Tehuantepec in Oaxaca, Mexico (but according to Olson and Caira (2001), this shark was misidentified and probably belongs to A. pelagicus). Subsequently, Litobothrium amplificum was redescribed by Olson and Caira (2001) based on 17 worms obtained from A. pelagicus from the Gulf of California. This new record extends the geographic distribution of this cestode.

Litobothriidea Dailey, 1969 Taxonomy

Litobothrium amplificum was originally described as a member of Renyxa by Kurochkin and Slankis (1973). However, Euzet (1994) considered this genus to be a synonym of Litobothrium.

Litobothrium amplificum can be distinguished from 5 of the 8 remaining species included in the genus by having 4 cruciform pseudosegments in the scolex while L. amsichensis (see Figure 3), L. daileyi, and L. nickoli each have 5, and L. coniformis and L. gracile each have 3 pseudosegments. Litobothrium alopias and L. janovyi share the same number of pseudosegments with L. amplificum; however, the fourth cruciform pseudosegment of L. amplificum has recurved laciniations and medial projections that are absent in the other 2 species (Olson and Caira, 2001). Litobothrium aenigmaticum, the most recently described species for the genus, differs from all the other species because it has a dome-shaped, grooved scolex, while in the other species, the scolex is constituted of an apical sucker and several cruciform pseudosegments without glandular tissue (Olson and Caira, 2001; Caira et al., 2014a).

The establishment of this order was strongly supported by molecular phylogenetic analyses that included broad sampling of cestodes belonging to several orders (Waeschenbach et al., 2012; Caira et al., 2014b). In both studies, litobothriideans were recovered as the sister taxon of the clade that includes the acetabulate cestode orders and as a monophyletic order. Intraorder relationships show that the clade formed by Litobothrium aenigmaticum + L. amplificum was robustly supported as the sister taxon of L. nickoli. This is interesting because all the members of this clade parasitize pelagic thresher sharks and have L. janovyi as a sister taxon, whose host is a different species (the bigeye thresher shark). In this context, future molecular phylogenetic studies could reveal that L. alopias, L. daileyi, and L. coniformis are closely related to L. janovyi since they share the same host species. On the other hand, L. gracile (hosted by the sand shark) and L. amsichensis (a parasite of the goblin shark) could constitute independent groups of the other 7 species.

Figure 3. Scolex and proglottids of Litobothrium amischensis Caira & Runkle, 1993, holotype specimen from the Queensland Museum, South Brisbane, Queensland, Australia. See the site at the link for the Queensland Museum for more information about this specimen.
(Source: Queensland Museum, 2023. License: CC BY.)

It is important to mention that the sequences of partial 28S rDNA (D1–D3) obtained from Litobothrium aenigmaticum and L. amplificum by Caira and colleagues (2014a) were identical; so, inclusion of other molecular markers is necessary for future studies.

Life Cycles

The life cycles of elasmobranch cestodes are practically unknown (Caira and Jensen, 2014); however, authors such as Caira and Reyda (2005) suggested that the life cycle of this group follows a pattern similar to other elasmobranch cestodes. The life cycle can include 2 or 3 intermediate hosts and larvae are trophically transmitted. In some cases, they can infect paratenic hosts (Caira and Jensen, 2014). Particularly, litobothriidean species only have been found parasitizing 4 species of lamniform sharks, among them members of Alopiidae (thresher sharks), Mitsukurinidae (goblin shark), and Odontaspididae (sand tiger sharks) (Caira and Jensen, 2014).

Additional Notes about the Morphology

The litobothriidean scolex consists of an apical sucker followed by a series of pseudosegments, a subset of which are cruciform (Caira and Jensen, 2014). However, these features are not present in most recently described species for the genus, namely, Litobothrium aenigmaticum. In contrast, this species exhibits a scolex consisting of a dome-shaped, grooved scolex proper and an extensive cephalic peduncle. In addition, the analysis of histological sections has revealed 4 distinct tissue types not seen in other litobothriideans.

When Caira and colleagues (2014a) described Litobothrium aenigmaticum, they pointed out that this species was the only hyperapolytic one so far in the order; nevertheless, these authors suggested that this material could represent a larval stage due to the lack of mature proglottids. The correspondence of microtriche distribution between adults and early juveniles corroborates that type specimens truly represent adult stages and ratify the hyperapolysis in this group for the first time (Caira et al., 2017b).

In spite of the remarkable morphological differences between Litobothrium aenigmaticum and the remaining 8 species included in this genus, molecular data robustly place it among the species in this order (Caira et al., 2014a).

Phyllobothriidea Caira et al., 2014 (Order)

Introduction

These acetabulate cestodes are parasites of the spiral valve or spiral intestine of sharks and occasionally batoid rays. Previously included in the Tetraphyllidea (Caira and Jensen, 2014), this order is named after the genus Phyllobothrium (from the Greek phyllon = leaf-shaped and bothros = trench) and was not formally recognized until the phylogenetic analysis with molecular data conducted by Caira and colleagues (2014b). These worms are characterized by unarmed bothridia harboring apical suckers, their body size (which can be from small to medium), and their spectacular ornamentation on the scolex (Caira and Jensen, 2014; Ruhnke et al., 2017). Only the members of the former Phyllobothriidae are included in this order, bearing 73 species in 24 described and valid genera, plus 3 genera yet to be described. Paraorygmatobothrium is the most speciose and geographically widespread genus, with 25 formally described species and 4 still-undescribed taxa (Cutmore et al., 2017; Ruhnke et al., 2017). In general, these cestodes exhibit a cosmopolitan distribution, but the records are less common at higher latitudes (Caira and Jensen, 2014).

Main Morphological Characteristics

Phyllobothriidea Caira et al., 2014 are polyzoic worms of small to medium size. They are hermaphroditic. Most of the species are euapolytic or anapolytic; just a few exceptions are hyperapolytic. They may be craspedote or acraspedote with spinitriches restricted to the bothridial surfaces, often being serrate or gongylate. The neck and the strobilar surfaces are filled with filitriches distributed in scutes or in leaf-like structures. The scolex has 4 unarmed muscular bothridia and an anterior accessory sucker. Stalks are absent and an accessory sucker lacks lateral muscular projections. They do not include facial loculi, although some can show marginal loculi. Some species can present laciniated proglottids. There is 1 set of reproductive organs on each proglottid. They have 2 pairs of lateral osmoregulatory canals; in general, the ventral canals are wider than the dorsal ones. There are numerous testes, and a post-poral field is almost always present. The vas deferens is convoluted. An external seminal vesicle may be present or absent. The cirrus is armed with spinitriches. The genital pore is lateral and alternates irregularly, and is mainly located in the anterior half of the proglottid. The vagina opens anterior to the cirrus sac into the genital atrium. The vitellarium is follicular and the follicles are usually arranged in lateral fields, occasionally circumcortically or circummedullarly. The uterus lacks lateral diverticula (Ruhnke, 2010; Caira et al., 2014b; Ruhnke et al., 2017).

Description and Summary of a Representative Species

Note: This work is not intended for the purposes of zoological nomenclature.

Paraorygmatobothrium prionacis (Yamaguti, 1934) Ruhnke, 1993

These are tetrabothridiated worms of medium body size (7.2–19.3 mm-long with a maximum width of 400–750 mm at the level of the scolex), and they are craspedote and apolytic. The number of segments is variable, from 11 to 29. The scolex measures from 430 to 620 mm-long and the apical area is covered with filitriches. The bothridia measure from 420 to 620 mm-long and 270 to 440 mm-wide. Each bothridium bears a single loculus and a round, anterior apical sucker (80–118 mm in diameter). The proximal surfaces of the bothridia are covered with serrated spinitriches and filitriches. On the distal locular surface and distal surface of the apical sucker, the serrated spinitriches are slender and filitriches are also present. The neck varies from 1.8 to 4.6 mm-long; its dorsal and ventral surfaces are scutellated with small (< 500 nm) overlapping triangular structures covering the surface. The mature segments are longer than they are wide (generally 3 times), with dorsal and ventral pairs of excretory ducts. A pair of nerve chords is situated laterally. The testes are arranged in 2 irregular longitudinal rows, from 2–4 in number in a horizontal row above the genital pore and 2–3 in number in a horizontal row below the genital pore; they are medullar, 1 row deep in cross section. The genital pores are lateral and alternate irregularly. The vagina is median, extending anteriorly the from ovary to the mid-level of the segment, then laterally along the anterior margin of the cirrus sac to the genital pore. The ovary is near the posterior end of the proglottid and is H-shaped in the frontal view and tetralobed in cross section. The uterus is ventral to the vagina and extends from the anterior margin of the ovary to the posterior margin of the cirrus sac in mature proglottids. A uterine duct is present, median, parallel, and dorsal to the uterus. The vitellarium is follicular and arranged in 2 lateral fields, each constituting 1–2 dorsal and 1–2 ventral columns, interrupted by the ovary and the cirrus sac. The eggs are spindle-shaped (Ruhnke, 2010).

Taxonomic summary

Type host: Blue shark Prionace glauca Linnaeus, 1758 (Carcharhiniformes).

Site of infection: Spiral intestine.

Type locality: Pacific coast, Japan.

Type specimens deposited: Unknown.

Phyllobothriidea Caira et al., 2014 Taxonomy

The taxonomic history of this group has been difficult to ascertain since some of the genera and species were originally only loosely defined (Ruhnke, 2010). Morphologically, the genus Paraorygmatobothrium is defined by the possession of bothridia with a single apical sucker and an undivided oval posterior loculus; likewise, this genus has serrate gladiate spinitriches on the proximal bothridial surface, the subterminal and terminal proglottids are longer than they are wide, they possess post-vaginal testes, and have vitelline follicles that are distributed in 2 lateral fields (Cutmore et al., 2017). Among the 25 species that belong to the genus, Paraorygmatobothrium prionacis has an apical sucker of 80 to 118 μm in diameter, a range that is similar to those registered from P. exiguum, P. janinae, P. triacis, P. sinclairtaylori, and P. ullmanni (Ruhnke, 2010; Cutmore et al., 2017). From these 5 species, P. prionacis can be distinguished due to its body size (7.2–19.3 versus 35–46 mm in P. triacis); from P. janinae¸ because this species has more proglottids (59–104 versus 11–29). Two other species have remarkable differences in relation to the number of testes: P. prionacis only has from 34 to 62 testes, while the number of testes is higher (57–152 and 86–116 testes, respectively) in P. sinclairtaylori and P. ullmanni. Finally, it can be separated from P. exiguum by the position of the genital pore along the proglottids (from 74–83% in this species versus 48–59% in P. prionacis) (Ruhnke, 2010; Cutmore et al., 2017). According to Cutmore and colleagues (2017), it is essential to analyze the molecular data for the Paraorygmatobothrium genus in order to understand their relationships; the description of species on the basis of morphological data alone is considerably problematic. However, the last analysis published by them using molecular evidence, does not show this genus as a monophyletic group (see Cutmore et al., 2017).

Despite the fact that the molecular data analysis is derived from the elevation of this family to the order level, the phylogenetic relationships among the Phyllobothriidea with respect to the other acetabulated clades such as Onchoproteocephalidea, the residual tetraphilideans, and the clade that comprises mainly cestodes of terrestrial hosts (Cyclophyllidea, Tetrabothriidea, Nippotaeniidea, and Mesocestoides) requires further investigation and expansion of the collecting sites as well as an increase in the number of species examined because fewer than 30% of the valid taxa have been put into a molecular phylogenetic context (Caira and Jensen, 2014; Caira et al., 2014b; Ruhnke et al., 2017; Waeschenbach et al., 2017).

Life Cycles

The Carcharhiniformes sharks harbor the majority of species of this cestode group, but they can also parasitize species of the Pristiophoriformes, Squaliformes, Orectolobiformes, and Lamniformes. Just a few phyllobothriideans have been found inhabiting the spiral valve of batoids (Myliobatiformes, Torpediniformes, and Rajiformes). Some authors have considered that this occurrence underlies a host-capture event, particularly since Chimaerocestos has been found to parasitize Chimaeriformes. In spite of the great richness of hosts, these worms are considered to be oioxenous (Ruhnke and Workman, 2013; Caira and Jensen, 2014; Caira et al., 2014b; Ruhnke et al., 2017). The recent discovery of species of this group from the Southern African marine realm by Ruhnke and colleagues (2017) expanded the distribution to all 12 marine realms considered by Spalding and colleagues (2007), making this group of parasites cosmopolitan.

According to Caira and Reyda (2005), the life cycle of the marine cestodes lacks free-living stages and the transmission between hosts depends on the particular food web dynamics. However, it is known that at least 2 or 3 intermediate hosts are involved. The work conducted by Jensen and Bullard (2010) allowed the identification of larval forms that could be assigned to what are now recognized as phyllobothriidean genera; these larvae were found only on teleost fishes that they considered to be acting as intermediate hosts involved in the life cycle of these parasites. Notwithstanding, recent observations have suggested the possibility that pinnipeds and cetaceans also serve as intermediate hosts of some species of this group, particularly in geographical regions where they represent the preferred prey of adult sharks (Klotz et al., 2018). This may help ratify the proposal about the high complexity of the web of intermediate-definitive hosts in the life cycle of these cestodes (Jensen and Bullard, 2010).

Additional Comments on the Taxonomy of the Group

There is no doubt about the position of this group as an order of elasmobranch-hosted cestode. As mentioned before, this group was named after Phyllobothrium, the type genus of Phyllobothriidae. Curiously, the taxonomic status of this genus remains problematic: The majority of species (21) are considered incertae sedis, and only 5 species are considered to be valid (including the type species P. lactuca) (Ruhnke, 2010; Ruhnke et al., 2017) (see Figures 4 and 5). Further investigation should be conducted on these species to understand their relationships inside the order.

Figure 4. Guidus francoi sp. n. from Bathyraja magellanica (Philippi), line drawings. A) Entire mature worm (holotype MACN-Pa No. 739); B) entire gravid worm (paratype MACN-Pa No. 746/6); C) scolex (paratype MACN-Pa No. 743); D) bothridium attached to host tissue, muscular bothridial sphinchter contracted (paratype MACN-Pa No. 741/1); E) terminal portion of gravid strobila, ventral view (paratype MACN-Pa No. 746/6), longitudinal muscles partially drawn to allow the view of internal organs; F) cocoon.
(Source: Menoret and Ivanov, 2021. License: CC BY 4.0.)

Figure 5. Guidus magellanicus from Bathyraja magellanica (Philippi), line drawings. A) Entire gravid worm (holotype MACN-Pa No. 747); B) scolex (holotype MACN-Pa No. 747); C) cocoon; D) bothridium, muscular sphincter relaxed (paratype MACN-Pa No. 748/2); E) bothridium, muscular sphincter contracted (paratype IPCAS No. C-888).
(Source: Menoret and Ivanov, 2021. License: CC BY 4.0.)

Rhinebothriidea Healy et al., 2009 (Order)

Introduction

Species allocated to this order comprise small cestodes that occur in the spiral intestine (valve) of rays (Batoidea) recorded in marine and freshwaters around the world. Rhinebothriidea was historically included in the order “Tetraphyllidea” despite evidence that the members of this order represent an independent clade; however, the formalization of this order did not take place until the first decade of the 2000s (Healy et al., 2017).

Rhinebothriidea was created by Healy and colleagues (2009) based on molecular evidence. This analysis fully supports the monophyly of the rhinebothriideans, which was corroborated in subsequent works (Caira et al., 2014b; Ruhnke et al., 2015; Marques and Caira, 2016). Currently, the presence of stalked bothridia is the only morphological synapomorphy of this group. Other morphological characters such as the presence of a cirrus armed with spinitriches, a follicular vitellarium, and a posterior ovary, have sometimes been considered to be important features to identify members of Rhinebothriidea; however, these traits are also found in other elasmobranch-hosted cestodes (Ruhnke et al., 2017) (for example, see Figure 6).

This order is composed of 4 families: Anthocephaliidae, Echeneibothriidae, Escherbothriidae, and Rhinebothriidae. The first family includes the genera Anthocephalum (with 22 species), Barbeaucestus (4 species), Cairaeanthus and Divaricobothrium (2 species each), and Sungaicestus (which is monotypic). The second family is composed of the genera Clydonobothrium, Echeneibothrium, Notomegarhynchus, Pseudanthobothrium (with 2, 50, 2 and 5 species, respectively) as well as the monotypic Tritaphros. Escherbothriidae is formed by the monotypic genus Escherbothrium and Stillabothrium (7 species). The last family contains 8 genera, 2 of them monotypic: Biotobothrium and Crassuseptum; Rhabdotobothrium and Spongiobothrium (with 2 species each); and Rhodobothrium and Scalithrium (including 7 species each). Rhinebothrium and Rhinebothroides are the most diverse genera of the family, with 49 and 8 species, respectively (Ruhnke and Seaman, 2009; Kornyushin and Polyakoya, 2012; Ruhnke et al., 2015; Reyda et al., 2016; Caira et al., 2017c; Herzog and Jensen, 2018).

Main Morphological Characteristics

The body is composed of 2 or more proglottids (making it polyzoic). The proglottids are hermaphroditic, with the posterior margin overlapping the next proglottid (craspedote) or not overlapping (acraspedote). Most species are euapolytic, but some are apolytic or hyperapolytic. Each segment contains 1 set of male and female reproductive organs. There are lateral osmoregulatory canals which are arranged in 2 pairs; the ventral canals are generally wider than the dorsal canals. A neck is absent. The scolex is armed with 4 muscular simple bothridia. The bothridia are stalked, mostly lacking differentiable apical suckers, and may either include marginal and/or facial septa (as in Anthocephalum and Echeneibothrium) or not (for example, in Stillabothrium cadenati). A myzorhynchus is present (for example, in Clydonobothrium, Echeneibothrium, Notomegarhynchus, Phormobothrium, Pseudanthobothrium, and Tritaphros) or absent (for example, in Barbeaucestus, Divaricobothrium, and Sungaicestus). The male reproductive system usually contains numerous testes or (rarely) just 2 testes (for example, as in some members of the genus Rhinebothrium, such as R. asymmetrovarium, R. biorchidum, and R. ditesticulum). Post-poral testes are usually lacking. The vas deferens is convoluted. An internal seminal vesicle is absent, while an external one may be present or not. The cirrus has spinitriches. The genital pore is lateral, and alternates irregularly. The vaginal opening is anterior to the cirrus sac opening into a genital atrium. The ovary is posterior and bi-lobed in cross section (as in Notomegarhynchus navonae) or tetralobed in cross section (as in Anthocephalum currani). The vitellarium is follicular and the follicles are arranged in lateral fields, sometimes displaced towards the median line of proglottids. The uterus is tubular and lateral diverticula may be present or absent, without pre-formed uterine pores (Healy, 2006; Healy et al., 2009; 2017; Ruhnke et al., 2015) See Figures 6–9 illustrating some of the characteristics of an example of Rhinebothrium sp.

Figure 6. Line drawings of Rhinebothrium paratrygoni Rego & Dias, 1976 collected from the type locality. A) Scolex of voucher (MZUSP 6214); B) terminal mature proglottid of voucher (MZUSP 6214). The vas deferens is above the cirrus sac. The arrow indicates the location of the section shown in the portion labeled Fig. 4; C) whole worm of voucher (MZUSP 6260k), illustrated in 3 fragments, from left to right: Anterior, middle, and posterior. The arrow indicates the anterior most mature proglottid. Abbreviations: CS) Cirrus sac; DOC) dorsal osmoregulatory canal; MG) Mehlis’ gland; O) ovary; T) testes; U) uterus; V) vitellaria; VA) vagina; VD) vas deferens; VS) vaginal sphincter; VOC) ventral osmoregulatory canal.
(Source: Reyda and Marques, 2011. License: CC BY.)

Species in this order can be distinguished from Amphilinidea and Gyrocotylidea by the shape of the scolex and due to the presence of a polyzoic body. Of the remaining 16 orders, Rhinebothriidea is separated by scolex conformation, since in this order, it bears 4 acetabulated and stalked bothridia (Healy et al., 2009).

Description and Summary of a Representative Species

Note: This work is not intended for the purposes of zoological nomenclature.

Anthocephalum currani Ruhnke and Seaman 2009

These comprise small-bodied worms (6.6–14.4 mm-long) composed of 35–70 proglottids that are slightly craspedote and apolytic. The scolex has 4 bothridia, 430–940 mm-wide. The bothridia are folded and pedicellate, each with 81–110 marginal loculi and a round anterior accessory sucker. The proximal surfaces of the loculi, bothridia, and bothridial rim are covered with spinitriches. Filitriches are present in the loculi and in the strobilar surface; the distal surfaces of the bothridia and accessory suckers covered also with slender spinitriches. The proglottids have the following measures: Immature (67–570 mm × 101–330 mm; length/width ratio 0.3–1.9:1), terminal and subterminal (580–1,700 mm × 134–410 mm; length/width ratio 1.9–9.4:1). The testes areoblong and are 37–50 in number at the terminal and subterminal  proglottids, arranged in 2–4 irregular columns, completely anterior to the cirrus sac. The cirrus sac is posteriorly recurved with a coiled cirrus armed with spinitriches. The genital pores are lateral and alternate irregularly. The vagina is sinuous and anteriorly extends to the Mehlis’ gland, then ventrally and laterally to the cirrus sac, and opens into the genital atrium anterior to the cirrus sac. The ovary is H-shaped in the frontal view and is tetra-lobed in cross section, and is located near the posterior end of the proglottid. The aporal lobe of the ovary is slightly longer than the poral lobe. The oviduct is spread out posteriorly to the level of Mehlis’ gland and is ventral to it. The oviduct extends posteriorly to the level of Mehlis’ gland and is ventral to it. The ovicapt is ventral at the posterior margin of the ovarian isthmus. The uterus extends from the anterior of the cirrus sac to the anterior end of the mature proglottids and is ventral to it. Two lateral bands of vitelline follicles are distributed from the anterior to the posterior end of the proglottid and the follicles are interrupted by the ovary. Each band consists of 3–5 dorsal and 3–5 ventral irregular columns of follicles (Ruhnke and Seaman, 2009).

Figure 7. Scanning electron micrographs of Rhinebothrium paratrygoni. Scolex, Figures A–G. A) Scolex; B) small letter indicates the locations of details shown in B–C and E. Proximal surface of the rim of the bothridium; C) proximal bothridial surface adjacent to the bothridial rim; D) proximal bothridial surface; E) transverse septum on the distal bothridial surface; F) stalk surface; G) strobila surface. Cirrus, Figures H–J. H) Free proglottid with everted cirrus; I) everted cirrus. Small letter indicates location of detail shown in J; J) coniform spinitriches and capilliform filitriches on the distal portion of the cirrus. Scale bars: A = 200 mm; B = 10 mm; C–G = 2 mm; H = 200 mm; I = 50 mm; J = 2 mm.
(Source: Reyda and Marques, 2011. License: CC BY.)

Figure 8. Cross section through a mature proglottid of Rhinebothrium paratrygoni at the level of the ovarian isthmus. Abbreviations: LM) Longitudinal muscles; MG) Mehlis’ gland; O) ovary; U) uterus; V) vitellaria; VA) vagina; VD) vas deferens.
(Source: Reyda and Marques, 2011. License: CC BY.)

Figure 9. Scoleces of Rhinebothrium copianullum. A) Scolex in which marginal longitudinal septa are visible, indicated by the white arrow; B) scolex in which marginal longitudinal septa are visible on the proximal bothridial surface, indicated by the white arrow. The white circle indicates the position of the marginal longitudinal septum on the distal surface. Scale bar: A–B = 200 mm.
(Source: Reyda and Marques, 2011. License: CC BY.)

Taxonomic summary

Type host: Bullseye stingray Dasyatis brevis.

Site of infection: Spiral intestine.

Type locality: Punta Arena (24° 04′ N, 109° 50′ W), Baja California Sur, Mexico.

Type specimens are listed here and additional details can be found in the original paper where this species was described: Holotype (CNHE 6234); paratypes (CNHE 6235; USNM 100993–100994; LRP 4241–4244).

Rhinebothriidea Healy et al., 2009 Taxonomy

To date, the genus Anthocephalum includes 22 valid species and A. currani differs from the rest of members based on the presence or absence of a number of features. For example, it differs from A. blairi, A. duszynskii, A. gravisi, A. hobergi, A. mounseyi, and A. odonnellae in total length (6.6–14.4 versus 2.5–4.9, 18–31, 1.8–3.7, 28, 2.6–3.4, and 11.6–20.1 mm, respectively); from A. alicae, A. blairi, A. cairae, A. centrurum, A. gravisi, A. haroldsoni, A. lukei, A. odonnellae, A. papefayei, and A. philruschi in the number of marginal loculi (81–110 versus 57–80, 65–73, 197–198, 71–80, 43–52, 41–57, 107–138, 135–159, 45–60, and 200–219, respectively). Anthocephalum currani can be distinguished from 12 other species based on the number of proglottids, since A. currani specimens have between 35–70 proglottids while A. alicae have 9–15, A. blairi have 13–21, A. cairae have 80–100, A. decrisantisorum have 20–33, A. duszynskii have 120–160, A. gravisi have 368–831, A. haroldsoni have 17–29, A. healyae have 150–171, A. mounseyi have 7–10, A. odonnellae have 86–120, A. papefayei have 106–177, and A. ruhnkei have 11–30. In the same way, the great number of testes of A. centrurum (47–78) allows separating it from A. currani, which has 37–50 testes. Eleven other species have a smaller number of testes per proglottid than A. currani: A. blairi (10–15 testes), A. decrisantisorum (17–24 testes), A. gravisi (23–38 testes), A. haroldsoni (25–32 testes), A. jensenae (14–20 testes), A. kingae (30–37 testes), A. meadowsi (15–25 testes), A. mounseyi (24–34 testes), A. papefayei (6–9 testes), A. philruschi (17–25 testes), and A. ruhnkei (22–34 testes). It also differs from A. centrurum and A. kingae in ovarian length (161–360 mm versus 390–710 mm and 376–440 mm, respectively). Testes in A. mattisi and A. michaeli are arranged in 2 regular columns while in A. currani they are grouped in 2–4 irregular columns (Ruhnke, 1994; 2011; Zamparo et al. 1999; Ruhnke et al., 2015; Marques and Caira, 2016; Herzog and Jensen, 2018).

Anthocephalum is now included within the Rhinebothriidea since the order was established, along with the genera Rhabdotobothrium, Rhinebothrium, Rhinebothroides, Scalithrium, Spongiobothrium, Echeneibothrium, and Rhodobothrium. Although the monophyly of rhinebothriideans in relation to the other acetabular cestode orders was strongly supported by 3 types of phylogenetic analyzes and 3 data partitions, Healy and colleagues (2009) refrained from establishing relationships at the family level until such time as the analyses included a large sample of taxa to provide a more accurate assessment of intraordinary relationships (Ruhnke et al., 2015). The work of Ruhnke and colleagues (2015) not only includes the description of 8 new species for Anthocephalum, but also designated to the family each of the clades that resulted from its analysis based on molecular data.

The subfamily Echeneibothriidae was elevated to the family level to include the genera Echeneibothrium and Pseudanthobothrium. This clade is unique because the apical organ (myzorhynchus) is retained in the adult stage. Rhinebothriidae was elevated from the subfamily to the family level to group the genera Rhabdotobothrium, Rhinebothrium, Rhinebothroides, Rhodobothrium, Scalithrium, and Spongiobothrium. The lack of apical suckers and lack of a definitive anterior/posterior orientation of the bothridia distinguishes this family from the remaining families. Anthocephaliidae was erected to include the genus Anthocephalum along with 4 other genera not described before. Members of this family exhibit a conspicuous anterior/posterior orientation signaled by the presence of an apical sucker in the bothridia and they have marginal loculi or 1 or more rows of facial loculi, and have vitelline follicles that are, in general, interrupted by the ovary. Escherbothriidae is characterized by facial loculi arranged in columns anteriorly and rows posteriorly rather than arranged in multiple rows, or may be entirely lacking, such as in members of Anthocephaliidae. Escherbothriidae was proposed to include the genus Escherbothrium and 1 undescribed taxon.

Life Cycle

Cestodes included in Rhinebothriidea exclusively parasitize batoid elasmobranchs. Most of the species described have been recovered from Myliobatiformes (stingrays and eagle rays), and in a smaller number of Rajiformes (skates), Rhinopristiformes (sawfishes), and Torpediniformes (electric rays) (Rhunke et al., 2017). The life cycle of species in this order of cestodes is poorly known because the identification of larvae at the species level (using morphology) is practically impossible as in other orders of elasmobranch-hosted cestodes. However, the results obtained by Jensen and Bullard (2010) using molecular and morphological data suggest that rhinebothriideans use some teleosts (members of Gadidae, Lobotidae, Paralichthyidae, Serranidae, and Sparidae) and molluscs (such as Donax variabilis) as intermediate hosts. Once these hosts are eaten by the definitive hosts (rays), the parasites reach sexual maturity in the spiral intestine and reproduce.

Zoogeography

The species in this order have a cosmopolitan geographical distribution. At the family level, the pattern of distribution seems to be related to the temperature of the waters: Echeneibothriidae seem to be restricted to temperate waters and Echeneibothriidae are restricted to tropical waters, while Anthocephaliidae and the Rhinebothriidae are found in both (Healy et al., 2017).

Species of rhinebothriideans can inhabit freshwater systems despite being predominately marine. In marine environments, the relationship between these parasites and their definitive hosts seems to be very strict and usually oioxenous. Notwithstanding, in freshwater systems, host range tends to be rather broad, and 1 species of cestode can parasite more than 1 host species. The relatively broad host range of some cestodes associated with freshwater rays may be due to the uniqueness of this relationship or to a recent event of colonization, but this hypothesis needs to be tested (Reyda and Marques, 2011). These authors provided an example of how this relationship appears in freshwater environments: Rhinebothrium, as R. copianullum and R. paratrygoni, each parasitize 8 and 7 potamotrygonid species,  respectively. Another singular case is Stillabothrium davidcynthiaorum, which was registered from 4 genera  of dasyatids as Brevitrygon, Himantura, and Maculabatis (Reyda et al., 2016). Reyda and colleagues (2016) also recorded the most extreme case of a non-oioxenous pattern, the species Stillabothrium cadenati was recovered from Rhinobatos rhinobatos (Rhinobatidae) and Zanobatus schoenleini (Zanobatidae), 2 species of hosts belonging to 2 different families. This is unusual because most members of this order have a 1:1 relationship with their hosts (that is, a very narrow host range), so that some species of cestodes can only be found in 1 species of host. The uniqueness of the exceptions to oioxeny is worth noting; and the questions related to the rupture of this pattern open a new perspective for further studies related to the ecology and evolution of the host-parasite relationship.

Relics of “Tetraphyllidea” van Beneden, 1850 (Order)

Introduction

The cestodes referred to the “Tetraphyllidea” (from the Greek tetra = 4, and phyllon = leaf-shaped) are so allocated because of the morphological characteristics of the scolex (the attachment organs) found in the spiral intestine and occasionally the stomach of species representing all orders of elasmobranch fishes. This group was proposed by van Beneden in 1850 to accommodate the family “Tetraphyllidés.” This family included cestode parasites with 4 lobes of the scolex that live in elasmobranchs. Under this name, van Beneden established 3 subgroups: Phyllobothriens (now Phyllobothriidea), phyllacanthiens (now Onchoproteocephalidea), and phyllorhynchiens (now Trypanorhyncha) (Euzet, 1994). Although van Beneden (1850a; 1850b) made the first taxonomic analysis of the group, he never considered it to be an order (Euzet, 1994). Subsequent to van Beneden, Braun (1894–1900) was the first author that considered Tetraphyllidea to be an order consisting of 4 families (Onchobothriidae, Lecanicephalidae, Phyllobothriidae, and Ichthyotaeniidae). Since then, the “Tetraphyllidea” has included cestode species that lack exclusive diagnostic characteristic as the other cestode orders hosted by elasmobranchs (Caira et al., 2017f). For this reason, orders such as Onchoproteocephalidea, Trypanorhyncha, Cathetocephalidea, Lecanicephalidea, Litobothriidea, Phyllobothriidea, and Rhinebothriidea have been derived from this group (Braun, 1894–1900; Olson and Caira, 2001; Caira et al., 2005; 2014b; Healy et al., 2009). Despite all these changes, “Tretraphyllidea” remains the most problematic order of Cestoda,  because it is not a monophyletic group and contains cestodes with morphology that varies remarkably from one another. Consequentially, the remaining taxa of “Tetraphyllidea”  require a phylogenetic analysis to establish accurate relationships (Caira and Jensen, 2014; Caira et al., 2014b).

Main Morphological Characteristics

“Tetraphyllidea” are polyzoic cestodes. The scolex of all species of “Tetrapyllidea” has 4 sessile or pedunculated bothridia,  but present in a great variety of forms. Some species of this order have hooks, loculi, or combinations of these. For example, species of Pedibothrium have 1 pair of anterior hooks that are bipronged, while in Yorkeria, Pachybothrium, and Spiniloculus the pair of hooks is unipronged (Caira and Pritchard, 1986; Caira et al., 2007; Desjardins and Caira, 2011). In contrast, species of Calliobothrium, Symcallio, Erudituncus, and Biloculuncus have 2 pairs of hooks; other species of “Tetraphyllidea” lack hooks. In genera such as Erudituncus and Biloculuncus, each bothridium is divided into 2 loculi, while in Calliobothrium and Symcallio, each bothridium is divided into 3 loculi (Nasin et al., 1997; Healy and Caira, 2001; Bernot et al., 2015). Bothridia of Dioecotaenia cancellata and D. campbelli have 3 columns of facial loculi (Schmidt, 1969; Mayes and Brooks, 1980; Caira et al., 2017f). This feature is also present in Glyptobothrium zwerneri in which bothridia are divided into 3 longitudinal rows of loculi and separated into 3 parallel longitudinal rows of 10–12 loculi (Pulido-Flores and Monks, 2014). Members of other genera, such as Ceratobothrium and Dinobothrium, possess an apical pad (Caira et al., 2017f); in species of Rhoptrobothriidae, the cephalic peduncle bears 4 stalked extensions, termed remi by Jensen and Caira (2006); this feature is unique to this family.

The morphology of the strobila is very similar to members of Trypanorhyncha and Lecanicephalidea (Schmidt, 1986). Some species are euapolytic (such as Yorkeria hilli, Y. kelleyae, Caulopatera pagei, and Pedibothrium cabrali) (Caira and Tracy, 2002; Caira et al., 2004; Cutmore et al., 2010), hyperapolytic (such as Calliobothrium australis (Ivanov and Brooks, 2002)), or apolytic (such as Symcallio barbarae) (Ivanov and Brooks, 2002)). The proglottids can be acraspedote (Cutmore et al., 2010; 2018; specifically, Yorkeria, Caulopatera, and Carpobothrium, according to Caira and Tracy (2002); Koontz and Caira (2016)) or craspedote (specifically, Calliobothrium and Symcallio; see Ivanov and Brooks, 2002; Bernot et al., 2016)). The genital pores are lateral or sublateral (as in Duplicibothrium; Williams and Campbell, 1978; Ruhnke et al., 2000) and alternate irregularly. There are numerous testes and the vagina opens anterior to the cirrus sac. The ovary is posterior and bi-lobed or tetralobed in cross section. The vitelline follicles are arranged in 2 lateral bands.

Currently, “Tetraphyllidea” includes 6 families and 4 clades, as recognized by Caira and others (2014b) and described by Caira and others (2017f): Balanobothriidae is the family with the most species with 38, distributed in 5 genera, followed by Calliobothriidae (26 species and 4 genera), Clade 4 (9 and 3, respectively), Clade 2 (8 and 1, respectively); Rhoptrobothriidae and Serendipidae (both with 6 species and 3 genera); Clade 3 (with 3 species of Carpobothrium and the monotypic Caulopatera; Gastrolecithidae with the genera Cerabothrium (1 species) and Dinobothrium (3 species); Clade 1 (with 3 monotypic genera), and, finally, Dioecotaeniidae with the genus Dioecotaenia, constituting 2 species. Up until the latest classifications, “Tetraphyllidea” included 106 species and 27 genera (Caira et al., 2017f).

Description and Summary of a Representative Species

Note: This work is not intended for the purposes of zoological nomenclature.

Duplicibothrium cairae Ruhnke et al., 2000

The worms are slightly craspedote and euapolytic. The scolex of this species has 4 pyriform bothridia. The dorsal and ventral bothridia are paired and fused. The bothridia each have 27–33 loculi arranged in 5 or 7 anterior rows of 3, 1 posterior row of 5, and the last posterior row with 7. The scolex is covered with round microtriches; the cephalic peduncle is  covered with dense microtriches.

There are 20 to 35 proglottids per strobila, progressively becoming longer than wider. The last segments have dorsal and ventral pairs of excretory ducts. The mature segments have 28–43 testes distributed in a post-ovarian field. In cross section, there are 4–10 medullary testes in 2 irregular deep rows. The cirrus is armed with spiniform microtriches. The cirrus sac is oval. The genital pore is positioned within 80–96% of the proglottid length, irregularly alternating and sublateral. The vagina is weakly developed in the mature proglottids. The ovary is digitiform in cross section. The uterus is median and poorly developed in the terminal proglottids. There are 8–12 vitelline follicles that are convergent in a dorsal field and are not found at the level of the ovary and cirrus sac (Ruhnke et al., 2000).

Taxonomic summary

Type host: Pacific cownose ray Rhinoptera steindacheneri Evermann and Jenkins, 1891.

Site of infection: Spiral intestine.

Type locality: Puertecitos (28° 85′ 50″ N, 113° 83′ 20″ W), Baja California, Gulf of California, Mexico.

Type specimens are listed here and additional details can be found in the original paper where this species was described: Holotype (CNHE 3846); paratypes (CNHE 3847; USNM (USNPC) 89726, 89727; HWML (15275, 15276).

“Tetraphyllidea” van Beneden, 1850 Taxonomy

To date, Duplicibothrium contains 3 species: D. cairae, D. minutum, and D. paulum, all of them parasites of rays of the genus Rhinoptera (Caira et al., 2017f). Duplicibothrium is characterized by the possession of 4 bothridia, the dorsal and ventral fused lengthwise into 2 pairs; the bothridial surfaces are divided into loculi by muscular septa or horizontal and longitudinal septa, showing a digitiform ovary and sublateral genital pore (Williams and Campbell, 1978; Ruhnke et al., 2000). Duplicibothrium cairae possesses a pair of longitudinal septa on each bothridium, while in D. minutum and D. paulum this feature is absent. Each septum is bifurcated in the posterior third of the bothridia, forming 5 or 7 anterior horizontal rows and ending with 1 row of 5 loculi and 1 moreposterior row of 7 loculi. Duplicibothrium cairae differs from the other 2 species by the number of segments: D. paulum has 3–11 proglottids, D. cairae has 20–35 proglottids, and D. minutum has 6–14 proglottids. In addition, D. cairae can be distinguished from D. paulum and D. minutum by the number of loculi in the bothridia; D. paulum has 57–63 loculi per bothridia, and D. minutum has 6–8 loculi per bothridia versus 27–33 per bothridia in D. cairae (Williams and Campbell, 1978; Ruhnke et al., 2000).

In the latest phylogenetic analysis of Duplicibothrium, the represented species nested with Glypthobothrium and Serendip, which are included in Serendipidae (Caira et al., 2017f). According to this, the phylogenetic position of Duplicibothrium is strongly supported by morphological and molecular evidence, due the 3 genera of Serendipidae being characterized by the presence of facial loculi in the bothridia (Ruhnke et al., 2000).

“Tetraphyllidea” does not represent a monophyletic group. All phylogenetic analyses, both with morphological or molecular data that included species of this order, conducted since 1981 by Euzet and colleagues (1981) through Caira and colleagues (2014b), indicate that this order is paraphyletic (Olson and Caira, 1999; Caira et al., 1999; 2001; Waeschenbach et al., 2007; 2012). The resolution of this paraphyly is essential to understand cestode evolution and describe the phylogenetic  relations of species currently included in “Tetraphyllidea” (Caira et al., 2014b). The last analysis with molecular data of “Tetraphyllidea” shows that this group is non-monophyletic since its species were distributed across trees in different clades (Caira et al., 2014b; 2017f). For this reason, Caira and colleagues (2014b; 2017f) retained these species as members of “Tetrapyllidea” and suggested that more exhaustive studies should be conducted.

Finally, according to Caira and colleagues (2014b; 2017f), “Tetraphyllidea” contains 10 independent groups (see above). Interestingly, Clade 1 of this analysis is the sister taxon of Rhinetobothriidea and Clade 3 of Cyclophyllidea.

Life Cycle

The life cycle of tetraphyllidean cestodes is poorly known. Caira and Reyda (2005) and Caira and Jensen (2014) have suggested that species of “Tetraphyllidea” likely parasitize 2 or 3 intermediate hosts and 1 species of elasmobranch as definitive host. The adults of “Tetraphyllidea” have been reported  as hosts of all orders (8 of sharks and 4 of batoids) of Elasmobranchii. At the family level, tetrapyllideans are parasites of 23 families (Caira et al., 2017f). The larval stages have been recorded in crustaceans, molluscs, and fishes (Jensen and Bullard, 2010). To date, only the life cycle of the tetraphyllidean Calliobothrium verticillatum has yet been described; as an adult, it is a parasite of the spiral valve of the smooth dogfish Mustelus canis (Cherry et al., 1991). The plerocercoid larvae have been found parasitizing the lumina of the anterior and midgut ceca of the hermit crab Pagurus pollicaris (Cherry et al., 1991). This crab is an important component of the dogfish’s diet (Montemarano et al., 2016). In general, the life cycle of C. verticillatum begins when worms reach maturity in the spiral valve of M. canis. These cestodes produce hexacanth embryos that are released from gravid proglottids and are eaten by the hermit crab, where the procercoids and plerocercoids are developed. Finally, the hermit crabs are ingested by sharks that act as definitive hosts (McDermott et al., 2010).

According to Jensen and Bullard (2010), one factor that contributes to the scarcity of information on life cycles is that the larval stages lack the morphological characteristics of adults, which makes taxonomic identification difficult. Although molecular data have been used to match the larval stages with the adult forms, analyses are scarce. For this reason, there are many records of “Tetraphyllidea” larvae without specific identifications (Álvarez et al., 2002; Palm and Klimpel, 2008; Klimpel et al., 2010; Carballo et al., 2011; Montoya-Mendoza et al., 2014; Centeno-Chalé et al., 2015; Constela et al., 2015; Dallarés et al., 2017; Morales-Serna etal., 2017). The most complete analysis using molecular characters  for taxonomic identification of larvae was conducted by Jensen and Bullard (2010). In this analysis the authors identified larvae of Duplicibothrium minutum, Anthobothrium spp., and possibly Pedibothrium spp. The larval stages of D. minutum were collected from bivalves and gastropods (that is, Melongena corona and Angulus versicolor); larvae of Pedibothrium spp., were found in the fishes Opsanus beta and Lutjanus campechanus, and the larval stages of Anthobothrium spp. were found in fish such as Ariposis felis, Trichiurus lepturus, Peprilus burti, and Diplectrum formosum. According to Jensen and Bullard (2010), these organisms act as intermediate hosts for this group of cestodes since they are an important component of the diet of sharks. In addition, some species exhibit heteroxenous associations which allows them to parasitize more than 1 species of host (for example, Calliobothrium verticillatum), while other species of “Tetraphyllidea” exhibit oxioenus associations with their hosts. For example, some species of the genus Symcallio only parasitize sharks of the genus Mustelus (Bernot et al., 2015).

Caira and colleagues (2017f) pointed out that the geographical distribution of members in this order is determined by the geographical distribution of their hosts, although these cestodes only have been recorded between 60° N and 60° S latitudes, mainly in tropical localities, such as the Gulf of California (specifically, Duplicibothrium cairae (Runhke et al., 2000)).

Additional Relevant Details about the Order “Tetraphyllidea” van Beneden, 1850

Species of Calliobothrium and Symcallio present different site specificity along the spiral intestine (Bernot et al., 2015). Cislo and Caira (1993) analyzed the parasites of Mustelus canis and observed that S. lintoni and C. verticillatum each have a different site of attachment along the spiral intestine. Symcallio lintoni was found in the anterior of the spiral intestine whereas C. verticillatum was found in the posterior region.

The majority of species of Cestoda are hermaphroditic; however, there are few exceptions, such as species of Dioecotaenia. These species are the unique dioecious cestodes of “Tetraphyllidea,” and in both species, the strobila has separate sexes (the proglottids only have male genital organs or only female genital organs) (Schmidt, 1969; Mayes and Brooks, 1981). This feature is also present in some Cyclophyllidea as members of Dioecocestidae, parasites of charadriiform birds, and in the progynotaeiid Gynandrotaenia, which are parasites of flamingos (Olson and Caira, 1999; Mariaux et al., 2017).

Literature Cited

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Supplemental Reading

Costa, G., S. Cavallero, S. D’Amelio, L. Piaggi, et al. 2011. Helminth parasites of the Atlantic chub mackerel, Scomber colias Gmelin, 1789 from Canary Islands, Central North Atlantic, with comments on their relations with other Atlantic regions. Acta Parasitologica 56: 98–104. doi: 10.2478/s11686-011-0006-1

Klimpel, S., M. W. Busch, T. Sutton, and H. W. Palm. 2010. Meso- and bathy-pelagic fish parasites at the Mid-Atlantic Ridge (MAR): Low host specificity and restricted parasite diversity. Deep-Sea Research, Part I: Oceanographic Research Papers 57: 596–603. doi: 10.1016/j.dsr.2010.01.002

Ruhnke, T. R. 2011. A monograph on the Phyllobothriidae (Platyhelminthes, Cestoda). University of Nebraska State Museum 25, 205 p.