J. Parasitol., 100(4), 2014, pp. 373–391 Ó American Society of Parasitologists 2014

A DIGEST OF ELASMOBRANCH TAPEWORMS

Janine N. Caira and Kirsten Jensen* Department of Ecology & Evolutionary Biology, 75 N. Eagleville Rd., University of Connecticut, Storrs, Connecticut 06269-3043. Correspondence should be sent to: [email protected]

ABSTRACT: This review brings together decades of work on elasmobranch tapeworms. The field has advanced significantly over the past 20 yr, with an emphasis on the discovery and description of novel taxa, and the establishment of phylogenetic frameworks for individual orders and their interrelationships. Tapeworms parasitizing elasmobranchs represent 9 orders and include 977 species and 201 genera—over 250 species and 50 genera are new within the last 2 decades. The 9 orders are treated individually, highlighting recent assessments of phylogenetic relationships informed by molecular sequence data. All but the ‘‘Tetraphyllidea’’ are monophyletic. Although much remains to be learned about their interrelationships, existing phylogenetic hypotheses suggest that elasmobranch tapeworms have played a key role in the evolution of the cestodes of essentially all other vertebrate groups. The apical organ is a defining feature (i.e., a synapomorphy) of a clade consisting of acetabulate taxa and Litobothriidea. Novel hook amino acid composition data support the independent origin of hooks in the various groups of hooked tapeworms. Cestode records exist for representatives of most of the major groups of elasmobranchs, however skates (Rajiformes) and catsharks (‘‘Scyliorhinidae’’) are particularly neglected in terms of species sampled. The majority of tapeworm species are extremely host-specific exhibiting species- specific (i.e., oioxenous) associations with their hosts. Rapid advancements in elasmobranch taxonomy, with over 300 of the 1,200 species appearing new in the past 20 yr, signal the need for careful attention to be paid to host identifications; such identifications are best documented using a combination of specimen, photographic, and molecular data. Above the species level, many cestode taxa are restricted to host orders, families, or even genera. Documentation of these affiliations allows robust predictions to be made regarding the cestode faunas of unexplored elasmobranchs. Trypanorhynchs are the notable exceptions. Life cycles remain poorly known. Recent applications of molecular methods to larval identifications have reinvigorated this area of research. Tapeworms are more diverse in elasmobranchs of tropical and subtropical waters, but they occur globally not only at the poles and in deep waters, but also in freshwaters of South America and Southeast Asia. The cestode faunas of batoids are much more speciose and complex than those of sharks. The faunas of deeper water sharks are particularly depauperate. The tapeworms of elasmobranchs and their hosts are now among the most well documented host-parasite systems in existence. This system has not yet reached its potential as a resource for investigations of basic ecological and evolutionary principles.

The tapeworms that parasitize elasmobranchs (i.e., sharks and suckers. Cestode orders vary in diversity from fewer than 10 to rays) exhibit a spectacular variety of forms (Fig. 1A-J). hundreds of species (Fig. 2). All but the ‘‘Tetraphyllidea’’ are Interpretations of the relationships underlying these forms have almost certainly monophyletic. With a few exceptions, elasmo- varied substantially and have manifested in divergent higher branch tapeworms are moderate in size relative to other cestode classification schemes. For example, Schmidt (1986) recognized 6 groups, with most species ranging in length from 500 lm to 60 cm. orders (Dioecotaeniidea, Litobothriidea, Diphyllidea, Lecanice- Members of some orders exclusively parasitize sharks, others phalidea, Tetraphyllidea, Trypanorhyncha), but Khalil et al. exclusively batoids, and some parasitize both groups. Almost all (1994) recognized only the latter 4 orders. Historically, there has reside in the spiral intestine of their hosts. The majority of species been a tendency to group cestodes exhibiting these relatively occupy marine environments; the exception is the Onchoproteo- disparate morphological forms together in higher-level classifica- cephalidea as only a subset parasitizes elasmobranchs and many tions, perhaps in part because of their shared associations with occur in freshwater. In all but the Trypanorhyncha, host fidelity elasmobranchs. However, over the past 2 decades, substantial at the species level is usually strict. For context and because the inroads have been made in our understanding of the evolution, taxonomy and systematics of these groups has been moving classification, and host associations of these parasites. In total, forward so rapidly, a brief synopsis of each of the 9 orders as they 977 species and 201 genera are now recognized; approximately are currently configured is provided below. 250 of these species and 50 genera have been erected over the past 2 decades alone. It is beyond the scope of this review to treat all of CATHETOCEPHALIDEA Schmidt & Beveridge, 1990 these taxa; instead readers are referred to the Global Cestode (Fig. 1F) Database (www.tapewormdb.uconn.edu) for information on individual species and genera and to Caira et al. (1999) for a With only 7 valid species and 3 valid genera the Cathetoce- detailed treatment of the terminology applied to the morpholog- phalidea is one of the least speciose elasmobranch cestode orders. ical features of these groups. Here we review current assessments Its members are characterized by a scolex that lacks bothria or of the diversity and evolution of tapeworms of elasmobranchs, acetabula, and instead consists of an anterior globose or their host associations, and the key role they have played in the transversely extended region and a posterior rugose base with evolution of cestodes overall. or without a band of papillae. Species are moderate in size Tapeworms of elasmobranchs are now considered to constitute ranging in total length from 3–10 cm. Cathetocephalideans are 9 of the 19 cestode orders. With the exception of litobothriideans oioxenous, sensu Euzet and Combes (1980); each species and cathetocephalideans, they are generally divided into bothriate parasitizes a different species of carcharhinid shark, specifically or acetabulate forms based on scolex morphology; acetabulate of the genera Carcharhinus and Lamiopsis. Collectively, these forms are further characterized as bearing bothridia or simple records indicate an essentially circumglobal distribution. The order was established by Schmidt and Beveridge (1990) for * Department of Ecology and Evolutionary Biology and the Biodiver- Cathetocephalus. It was expanded to include Sanguilevator by sity Institute, University of Kansas, Lawrence, Kansas 66045. Caira et al. (2005), and most recently, to also include Disculiceps DOI: 10.1645/14-516.1 (see Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014).

373 374 THE JOURNAL OF PARASITOLOGY, VOL. 100, NO. 4, AUGUST 2014

FIGURE 1. Scanning electon micrographs of scoleces of species representing 9 orders of elasmobranch tapeworms. (A) Diphyllidea (Halysioncum bonasum ex Rhinoptera bonasum). (B) Trypanorhyncha (Rhinoptericola megacantha ex R. bonasum). (C) Litobothriidea (Litobothrium nickoli ex Alopias pelagicus). (D) Lecanicephalidea (Seussapex karybares ex Himantura uarnak 2 sensu Naylor, Caira, Jensen, Rosana, White, and Last, 2012). (E) Rhinebothriidea (Rhabdotobothrium anterophallum ex Mobula hypostoma). (F) Cathetocephalidea (Disculiceps sp. ex Carcharhinus limbatus). (G) Phyllobothriidea (Paraorygmatobothrium sp. ex Carcharhinus brevipinna). (H) Onchoproteocephalidea (Acanthobothrium sp. ex Narcine entemedor). (I) ‘‘Tetraphyllidea’’ (Calliobothrium schneiderae ex Mustelus lenticulatus). (J) ‘‘Tetraphyllidea’’ (Pedibothrium brevispine ex Ginglymostoma cirratum). Abbreviations: H, hooks. CAIRA AND JENSEN—ELASMOBRANCH TAPEWORM DIGEST 375

lished by Marques et al. (2012) for weakly armed taxa from catsharks. Caira, Marques et al. (2013) published a reconfigura- tion of the order, aimed at the circumscription of monophyletic genera, that led to the erection of the additional genera Andocadoncum, Coronocestus,andHalysioncum. Collectively, these 6 genera comprise 56 valid species. Genera range in diversity from 1 species (i.e., Ahamulina and Andocadoncum) to 30 species (i.e., Echinobothrium) (Kuchta and Caira, 2010; Caira, Marques et al., 2013). The diphyllidean scolex is characterized by its possession of 2 bothria (sensu Caira et al., 1999), an apical organ that may or may not bear apical hooks and sometimes also lateral hooklets, may or may not possess a corona of spines, and a cephalic peduncle that may or may not be armed with 8 columns of spines. Diphyllideans are generally among the smallest of elasmobranch cestodes. Many species are less than 5 mm in total length (e.g., Probert and Stobart, 1989), although some several cm in total length are known (e.g., Khalil and Abdul-Salam, 1989). The order’s association with batoids, and in particular stingrays, guitarfish, and skates, is well recognized (Tyler, 2006). But, the importance of carcharhiniform sharks of the families Triakidae (e.g., Ivanov and Lipshitz, 2006) and the non-monophyletic ‘‘Scyliorhinidae’’ (e.g., Rees, 1959; Marques et al., 2012; Caira, Marques et al., 2013) as hosts for the order should not be underestimated. Strict host specificity at the species level is predominant, but verified exceptions exist (e.g., Tyler, 2001). Diphyllideans are known from all major oceans, primarily between latitudes of 608N and 608S. The order is monophyletic. The position of the Diphyllidea, along with the other bothriate orders, outside of the acetabulate cestode orders is a consistent result of molecular phylogenetic analyses (Olson et al., 2001; Waeschenbach et al., 2007, 2012; Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014) (see Fig. 3). The number of taxa in candidate families of elasmobranch hosts that remain to be examined leads us to anticipate that the Diphyllidea is more speciose than recognized.

LECANICEPHALIDEA Wardle & McLeod, 1952 (Fig. 1D)

FIGURE 2. Pie chart depicting relative species and genus (in parentheses) With 116 valid species in 24 valid genera, the Lecanicephalidea diversity of elasmobranch tapeworm orders. Note that more than half of is 1 of the more specious orders of elasmobranch tapeworms. The the Onchoproteocephalidea parasitize vertebrates other than elasmo- scolex consists of 4 simple bothridia or suckers and, with few branchs. exceptions (e.g., Jensen, 2001), an apical structure. The order’s monophyly is supported by morphological (Caira et al., 2001) and The latter study supported a sister taxon relationship between molecular (Caira, Jensen, Waeschenbach, Olson, and Littlewood, Sanguilevator and Cathetocephalus. The latter 2 genera are housed 2014) data. Although a synapomorphy for the Lecanicephalidea is in the Cathetocephalidae; Disculiceps belongs to the Disculicepi- lacking, most species are distinctive in their possession of a vagina tidae. This order is deeply nested among the acetabulate orders of that opens into the genital atrium posterior (rather than anterior) cestodes in the trees of Caira, Jensen, Waeschenbach, Olson, and to the cirrus sac and a vas deferens that extends from the level of Littlewood (2014), suggesting its non-acetabulate scolex is a the ovary to the cirrus sac. Lecanicephalideans are generally less derived condition. The number of carcharhinid species that than 1 mm, but they range from 400 lm (e.g., Jensen, 2001) to remain to be examined for cestodes suggests the order is likely more than 6 cm (e.g., Butler, 1987) in total length. They primarily much more diverse than current records indicate. parasitize batoids, although some records from sharks exist (Caira et al., 1997; Jensen, 2005); all occur in the marine environment. DIPHYLLIDEA van Beneden in Carus, 1863 Among batoids, they have been reported from 12 of 23 families (Fig. 1A) and 3 of 4 orders; they are conspicuously absent from Rajiformes. With very few exceptions (e.g., Cielocha et al., 2014), species At the time of the Tyler (2006) monograph, this order was exhibit oioxenous specificity for their hosts. Generic diversity of considered to consist of only 2 valid genera (i.e., Ditrachybothri- lecanicephalideans is greatest in stingrays (Dasyatidae) and eagle dium and Echinobothrium). Ahamulina was subsequently estab- rays (Myliobatidae). The order has an affinity for warmer, coastal 376 THE JOURNAL OF PARASITOLOGY, VOL. 100, NO. 4, AUGUST 2014

FIGURE 3. Summary of cestode phylogenetic relationships modified from Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014; fig. 2); branches lacking support have been collapsed. Color-coded bars to right of tree indicate environments; vertebrate icons indicate major groups of vertebrates parasitized, non-elasmobranch host taxa are indicated as black silhouettes. Uncertainty in affinities of selected elasmobranch-hosted taxa and taxa that primarily parasitize birds and mammals is indicated with ‘‘?’’. Presence of hooks is indicated with a purple hash mark and associated figure number if amino acid profile data are given in Figure 4. Abbreviations: ‘‘TE’’, ‘‘Tetraphyllidea.’’ CAIRA AND JENSEN—ELASMOBRANCH TAPEWORM DIGEST 377 waters (i.e., between latitudes of 408N and 408S). It is circum- species that parasitize snakes, amphibians, and even a mammal. global in distribution; diversity is highest in Indo-Pacific waters. We will not treat these species here, and instead refer readers to de With 13 of the 24 genera established since 1995, an updated Chambrier et al. (2004). The mere 12 genera hosted by familial classification based on a robust phylogenetic analysis, elasmobranchs include a disproportionate amount of the diversity with representation beyond the 11 genera included by Caira, in the order (i.e., 213 of 580 species) largely because of the Jensen, Waeschenbach, Olson, and Littlewood (2014), is long speciose Acanthobothrium with more than 150 members. With the overdue. Furthermore, ongoing studies of lecanicephalideans, exception of Prosobothrium (see Olson et al., 2001), all 12 genera mainly from batoids of Southeast Asia, suggest that species level are characterized by their possession of 1 or 2 pairs of bothridial diversity in the order is substantially underestimated. hooks on each of their 4 bothridia. Species range in size from 1 mm to 15 cm. There is some evidence from molecular analyses LITOBOTHRIIDEA Dailey, 1969 (Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014) that (Fig. 1C) the taxa previously assigned to the Proteocephalidea represent a monophyletic group within the Onchoproteocephalidea. This This is the second least speciose of elasmobranch-hosted does not appear to be the case for the genera previously assigned cestode orders. The 9 species in the order are all members of to the ‘‘Tetraphyllidea.’’ With a few exceptions (e.g., Healy, 2003), the single genus Litobothrium. The suppression of the second elasmobranch-hosted onchoproteocephalidean species exhibit genus, Renyxa, by Euzet (1994) was supported by the molecular oioxenous specificity. But they are hosted by an eclectic selection analyses of Caira, Jensen, Waeschenbach, Olson, and Littlewood of elasmobranch groups, with an emphasis on carcharhiniform (2014). With 1 notable exception, the litobothriidean scolex sharks (i.e., the cestode genera Megalonchos, Phoreiobothrium, consists of an apical sucker followed by a series of pseudoseg- Platybothrium, Prosobothrium, and Triloculatum) and myliobati- ments, a subset of which is cruciform. The exception is L. form batoids (i.e., Acanthobothroides, Onchobothrium, Pinguicol- aenigmaticum, which beyond its possession of coniform spini- lum, Potamotrygonocestus and Uncibilocularis). However, New triches, bears absolutely no resemblance to its congeners, and in genus 8 of Caira, Jensen, Waeschenbach, Olson, and Littlewood fact, little resemblance to cestodes because reproductive organs (2014) parasitizes Rhinopristiformes. Of particular note is have yet to be found. Nonetheless, molecular data robustly place Acanthobothrium; it is unique among the 110 elasmobranch- it among the species in this order (Caira, Jensen, Waeschenbach, hosted acetabulate genera in that its species parasitize multiple and Littlewood, 2014). Typical litobothriideans range in size from orders of batoids and sharks. Given that many of the non-hooked approx. 1 to 9 mm; L. aenigmaticum from 14 to 32 mm. members of the order parasitize hosts in freshwaters, it is Litobothriideans are oioxenous; each species associates with only interesting that the elasmobranch-hosted groups include those a single species of lamniform shark. Among lamniforms, they are found in freshwater elasmobranchs (Potamotrygonocestus) as well restricted to Alopiidae (thresher sharks), Mitsukurinidae (goblin as those found in hosts that often occur in euryhaline habitats shark), and Odontaspididae (sand tiger sharks). As few species in (e.g., Acanthobothroides and New genus 8). By far the majority of these host families remain to be examined for cestodes, discovery records come from tropical and subtropical waters, but species are of many additional species seems unlikely. The order was known from latitudes above 608N (e.g., Manger, 1972). established by Dailey (1969) and is known only from the Pacific Ocean. It is considered to represent the sister taxon to the PHYLLOBOTHRIIDEA Caira, Jensen, Waeschenbach, acetabulate clade of cestodes (Caira, Jensen, Waeschenbach, Olson & Littlewood, 2014 Olson, and Littlewood, 2014) suggesting that its lack of scolex (Fig. 1G) acetabula represents an ancestral condition. In the not too distant past (e.g., Euzet, 1994), most of the ONCHOPROTEOCEPHALIDEA Caira, Jensen, Waeschenbach, ‘‘tetraphyllidean’’ non-hooked acetabulate genera were assigned, Olson & Littlewood, 2014 in many cases by default, to the family Phyllobothriidae. The (Fig. 1H) substantial morphological variation seen among this assortment of taxa was accommodated by the subfamily designations Representing a combination of taxa previously assigned to the Thysanocephalinae, Echeneibothriinae, Phyllobothriinae, Trilo- Proteocephalidea and most of those assigned to the ‘‘tetraphylli- culariinae, and Rhinebothriinae. To a large extent, the recent dean’’ family Onchobothriidae, this is the only cestode order that dismantling of the ‘‘Tetraphyllidea’’ (Healy et al., 2009; Caira, includes both elasmobranch-hosted genera as well as genera Jensen, Waeschenbach, Olson, and Littlewood, 2014) has hosted by other vertebrate groups. Despite the somewhat radical emerged from a series of studies critically evaluating the nature of recognition of these taxa as members of the same order, morphology of genera traditionally assigned to the Phyllobo- support for their common evolutionary history is compelling (e.g., thriidae (e.g., Ruhnke, 1993, 1994, 1996a, 1996b; Ivanov, 2008; Olson et al., 2001; Caira et al., 2005; Waeschenbach et al., 2007, Ruhnke and Caira, 2009). But it was also informed by the 2012; Caira, Jensen, Waeschenbach, Olson, and Littlewood, discovery and description of novel generic forms (e.g., Caira and 2014). A robust synapomorphy for the order has yet to be Durkin, 2006; Ivanov, 2006; Ruhnke, Caira, and Carpenter, 2006; identified, but the presence of gladiate spinitriches throughout the Caira et al., 2011; Ruhnke and Workman, 2013). In establishing length of the strobila is at least a candidate feature (Caira, Jensen, the Rhinebothriidea, Healy et al. (2009) removed the Rhine- Waeschenbach, Olson, and Littlewood, 2014). The order is bothriinae and Echeneibothriinae from the Phyllobothriidae. In dominated by genera that parasitize vertebrates other than his monograph, Ruhnke (2011) addressed the polyphyletic nature elasmobranchs (i.e., 71 of 83 genera). In fact, the majority of of the Phyllobothriidae and provided a more restricted concept of species parasitize freshwater fishes, but the order also includes the family. In that work, he also determined the taxonomic status 378 THE JOURNAL OF PARASITOLOGY, VOL. 100, NO. 4, AUGUST 2014 of essentially all species and genera that have historically been representation of 13 of the 20 genera and yielded 1 clade assigned to the family in the context of his revised definition. As a consisting of Anthocephalum and the 4 undescribed genera of result of their molecular phylogenetic analyses, Caira, Jensen, Healy et al. (2009), and a clade consisting of the remaining genera Waeschenbach, Olson, and Littlewood (2014) elevated the family except for Echeneibothrium. The position of the latter genus was to ordinal status. With only a few exceptions, the genera assigned unstable across analyses. The order is entirely restricted to, and to the order were consistent with those assigned to the family by broadly distributed across, batoids. Species have been reported Ruhnke (2011). In general, phyllobothriideans exhibit simple, from all myliobatiform families except Gymnuridae, Plesiobati- undivided bothridia each of which bears an apical sucker; some dae, and Hexatrygonidae; from all rhinopristiform families except (e.g., Orectolobicestus and Nandocestus) also bear marginal loculi. Rhinidae; and from all but the least speciose of the 3 families of Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014) Rajiformes, the Anacanthobatidae. None of the 4 families of considered as many as 24 genera and 72 species to belong to the Torpediniformes has been reported to host the order. The order is order. However, as their analyses included representation of only cosmopolitan in distribution, with greatest diversity in tropical 12 of these genera and apical suckers are seen in other cestode and subtropical regions. However, Pseudanthobothrium and orders (e.g., some Rhinebothriidea) uncertainty remains with Echeneibothrium appear to have a particular affinity for cooler respect to membership of the Phyllobothriidea. The majority of waters. Rhinebothriideans are common members of the faunas of taxa parasitize sharks, with an emphasis on Carcharhiniformes freshwater stingrays throughout South America (e.g., Mayes et (i.e., the cestode genera Alexandercestus, Doliobothrium, Hemi- al., 1981; Brooks et al., 1981; Reyda, 2008; Reyda and Marques, pristicola, Orygmatobothrium, Paraorygmatobothrium, Pelichni- 2011) and Borneo (Healy, 2006b). Specificity of marine species bothrium, Phyllobothrium, Ruhnkecestus, Scyphophyllidium, appears to be oioxenous. There is some evidence that specificy Thysanocephalum, and New genus 10 of Caira, Jensen, Wae- may be more relaxed in species occurring in the freshwaters of schenbach, Olson, and Littlewood, 2014); but also Pristiophor- South America (e.g., Reyda, 2008; Reyda and Marques, 2011). iformes (i.e., Bibursibothrium, Cardiobothrium,and Flexibothrium); Squaliformes (i.e., Bilocularia and Trilocularia); ‘‘TETRAPHYLLIDEA’’ Carus, 1863 Orectolobiformes (i.e., Orectolobicestus); and Lamniformes (i.e., (Fig. 1I, J) Marsupiobothrium). The few members that parasitize batoids are hosted by Myliobatiformes (i.e., Anindobothrium and Nandoces- The ‘‘tetraphyllideans’’ remain the most problematic of the tus); Torpediniformes (i.e., Calyptrobothrium); and Rajiformes cestodes associated with elasmobranchs from the standpoint of (i.e., Guidus). The unexpected occurrence of Chimaerocestos in their phylogenetic relationships and thus also with respect to holocephalans is considered to represent a host-capture event ordinal placement of a number of genera. All evidence indicates (Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014). that the 30 genera and their 90 constituent species that were Collectively, the phyllobothriideans exhibit essentially a cosmo- retained as ‘‘tetraphyllideans’’ by Caira, Jensen, Waeschenbach, politan distribution, but records are less common at higher Olson, and Littlewood (2014), do not represent a single latitudes. monophyletic group. Figure 3 illustrates the uncertainty in the phylogenetic relationships of the 21 genera they found to be RHINEBOTHRIIDEA Healy, Caira, Jensen, interspersed among the other cestode orders, a fact that is Webster & Littlewood, 2009 reflected in the diversity of morphologies they exhibit. As it (Fig. 1E) stands, the ‘‘Tetraphyllidea’’ comprises genera with bothridial hooks (e.g., Calliobothrium, Megalonchos, Yorkeria, Spiniloculus, Exciting progress has been made in the systematics of this Pedibothrium, Balanobothrium, and Pachybothrium), but that are group of cestodes in the last few years. Recognition of these taxa not necessarily each others’ closest relatives. Also included are in an order independent from the ‘‘Tetraphyllidea’’ was the result genera with a pair of bothridial muscular projections (e.g., of morphological work conducted by Healy (2006a) and Dinobothrium and Ceratobothrium) and genera (e.g., Rhoptro- molecular analyses presented by Healy et al. (2009). Rhine- bothrium and Myzocephalus) bearing scolex rami (sensu Jensen bothriideans resemble ‘‘tetraphyllideans’’ in their possession of a and Caira, 2006). Some genera exhibit scoleces that bear a striking scolex comprised of 4 bothridia, but rhinebothriidean bothridia resemblance to those of the Phyllobothriidea (e.g., Crossoboth- are distinctive in that they are borne on stalks. With the possible rium and Clistobothrium), other genera (e.g., Caulobothrium, exception of Pseudanthobothrium, bothridea each bear facial Duplicibothrium, and Dioecotaenia) have scoleces that bear a loculi and in many cases also an apical sucker. The larval apical strong resemblance to those of the Rhinebothriidea; but in neither organ degenerates in most species during transformation to the case do these genera group with the members of the order they adult stage. The exceptions are Pseudanthobothrium and Echenei- resemble. Presumably, analyses that will include additional bothrium; they retain this feature in the form of the adult molecular markers and denser sampling of these and the 9 myzorhynchus. The order includes 111 species in 20 genera remaining genera will help to resolve these relationships. The (including the 4 undescribed genera of Healy et al., 2009). majority of ‘‘tetraphyllidean’’ genera are associated with 5 orders Rhinebothriideans range in size from 1 mm to 3 cm in total of sharks: the lamniform families Lamnidae (i.e., cestode genera length. A family-level classification for the order is currently such as Clistobothrium and Ceratobothrium) and Cetorhinidae lacking, but reconfiguration of membership of the Rhinebothrii- (i.e., Dinobothrium); the carcharhiniform families Triakidae (i.e., nae and Echeneibothriinae, may serve to accommodate at least Calliobothrium), Carcharhinidae (i.e., Anthobothrium), and Hemi- some genera once the generic interrelationships are more fully galeidae (i.e., Megalonchos); the squaliform family Squalidae (i.e., understood. Both the analyses of Healy et al. (2009) and Caira, Trilocularia); the hexanchiform family Hexanchidae (i.e., Cross- Jensen, Waeschenbach, Olson, and Littlewood (2014) included obothrium); a large proportion is associated with the orectolobi- CAIRA AND JENSEN—ELASMOBRANCH TAPEWORM DIGEST 379 form families Brachaeluridae (i.e., Carpobothrium), Ginglymo- ily parasitizing, as their names suggest, batoids and sharks, stomatidae (i.e., Pedibothrium, Pachybothrium, and Balanoboth- respectively. These phylogenetic efforts demonstrated that some rium) and Hemiscylliidae (i.e., Yorkeria and Spiniloculus). The of the 15 families recognized by Palm (2004) (i.e., Lacistorhyn- batoid-hosted genera parasitize only Myliobatiformes, specifically chidae, Eutetrarhychnidae, Gymnorhynchidae, Gilquiniidae, and of the families Myliobatidae (i.e., Rhoptrobothrium and Myzoce- Otobothriidae) are not monophyletic and are in need of revision. phalus); Rhinopteridae (i.e., Duplicibothrium and Dioecotaenia) Given the ubiquity of trypanorhynchs across host taxa and and Dasyatidae (i.e., Caulobothrium and New genus 9). All geographies, the species diversity of this group to date is grossly evidence suggests that species in these genera exhibit oioxenous underestimated. specificity for their hosts. Further generalizations regarding the ‘‘tetraphyllideans’’ will be more meaningful in the context of a PHYLOGENETIC RELATIONSHIPS clearer picture of their true affinities. The reconfiguration of cestode classification, from the 4 orders TRYPANORHYNCHA Diesing, 1863 parasitizing elasmobranchs recognized by Khalil et al. (1994) (i.e., (Fig. 1B) Trypanorhyncha, Diphyllidea, Lecanicephalidea, and Tetraphyl- lidea) to the 9 orders treated above, is entirely a result of the The Trypanorhyncha is the most specious elasmobranch-hosted dismantling of the Tetraphyllidea. All phylogenetic analyses have cestode order; to date, 303 species in 81 genera are recognized as shown the latter order to be paraphyletic (e.g., Euzet et al., 1981; valid. A considerable number of species and as many as 14 genera Brooks et al., 1991; Hoberg et al., 1997; Mariaux, 1998; Caira et are known from larval stages in intermediate hosts, mainly al., 1999, 2001, 2005; Olson and Caira, 1999; Kodedova´et al., teleosts; the elasmobranch definitive host for these remains to be 2000; Olson et al., 2001; Waeschenbach et al., 2007, 2012; Caira, determined. Overall, the most specious genera in the order are the Jensen, Waeschenbach, Olson, and Littlewood, 2014). The formal tentaculariid Nybelinia with 28 species, and the eutetrarhynchid dismantling of the Tetraphyllidea occurred in stages. Olson and Dollfusiella with 26 species, whereas a number of genera (e.g., Caira (2001) resurrected the Litobothriidea of Dailey (1969). Fellicocestus, Mixodigma, and Nataliella) are monotypic. Trypa- Caira et al. (2005) resurrected the order Cathetocephalidea of norhynchs are characterized by their possession of a scolex with 2 Schmidt and Beveridge (1990). Healy et al. (2009) established the or 4 bothria and a complex rhyncheal apparatus including 4 new order Rhinebothriidea. The molecular phylogenetic analysis armed tentacles, tentacle sheaths, and retractor muscles. The of Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014), in rhyncheal apparatus is a true synapomorphy for the group, large part because of the breadth of its taxon sampling (i.e., 68 of although species in the genera Aporhynchus and Nakayacestus the 110 acetabulate genera parasitizing elasmobranchs) confirmed have secondarily lost this feature altogether. The smallest species these previous actions and resulted in establishment of the are approximately 1 to 2 mm in total length (see Palm, 2004), but additional new orders Phyllobothriidea and Onchoproteocepha- species longer than 30 cm are not uncommon (e.g., species of lidea. Unfortunately, despite all efforts to circumscribe mono- Sphyriocephalus, Nybelinia,andFellicocestus). Most species phyletic orders, several genera or groups of genera remain parasitize the spiral intestine of their elasmobranch host, but distributed among the established acetabulate orders, requiring some such as the Tentaculariidae reside in the stomach and a few retention of a paraphyletic ‘‘Tetraphyllidea’’ sensu stricto; the have been reported from the gall bladder (Fellicocestus)or affinities of these taxa with respect to one another and to all other nephridial system (Mobulocestus) (Campbell and Beveridge, 2006). The Trypanorhyncha is the only group of elasmobranch cestode orders are unclear because not only was support for their cestodes in which strict host specificity at the species level is not inclusion in any of the larger clades low, but they were also found the general pattern. Although some species have been reported to be labile in position across analyses by Caira, Jensen, from but a single host species, others parasitize elasmobranchs Waeschenbach, Olson, and Littlewood (2014). representing as many as 4 orders (see Palm, 2004; Palm and Caira, Nonetheless, resolution of some elements of the interrelation- 2008). Members of all but the following 7 shark and 5 batoid ships among the monophyletic elasmobranch-hosted orders has families have been reported to host trypanorhynchs: Echinorhi- resulted from efforts to explore cestode interrelationships overall nidae, Brachaeluridae, Rhincodontidae, Mitsukurinidae, Pseudo- (e.g., Olson et al., 2001; Waeschenbach et al., 2007, 2012; Caira, carchariidae, Proscylliidae, and Leptochariidae; and Narkidae, Jensen, Waeschenbach, Olson, and Littlewood, 2014). The more Anacanthobatidae, Platyrhinidae, Zanobatidae, and Hexatrygo- stable aspects of these are summarized in Figure 3. The bothriate nidae. Collectively, the Trypanorhyncha are likely the most orders, which include the trypanorhynchs and diphyllideans, cosmopolitan of elasmobranch-hosted cestode groups; they consistently group outside of the acetabulate orders, although parasitize elasmobranchs in both the marine and freshwater stability in their interrelationships has yet to be achieved. The environment. Even individual species have been demonstrated to Litobothriidea is sister to a robust clade consisting of the have a cosmopolitan distribution (Palm et al., 2007). Several acetabulate orders, a relationship supported by the presence of comprehensive treatments of the group have focused either on an apical organ at some time in development. The position of the classification (Dollfus, 1942; Campbell and Beveridge, 1994; cathetocephalideans among the acetabulate taxa in the analysis of Palm, 2004) or phylogenetic interrelationships based on molecular Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014) is sequence data (Palm et al., 2009; Olson et al., 2010). Historically, interesting given the unusual non-acetabulate scolex morphology classification schemes have differed depending on the importance of members of the order. This placement differs from that placed or tentacular armature versus other morphological presented by Caira et al. (2005), but it seems more probable given features by respective authors. As it stands, 2 suborders are that the analyses of Caira, Jensen, Waeschenbach, Olson, and recognized: the Trypanobatoida and Trypanoselachoida primar- Littlewood (2014) were based on both more data and a much 380 THE JOURNAL OF PARASITOLOGY, VOL. 100, NO. 4, AUGUST 2014 greater sampling of taxa. Among the acetabulate orders, the acetabula in the Cathetocephalidea and Nippotaeniidea is Lecanicephalidea is likely basal. considered to represent a loss in both cases. With respect to the other acetabulate groups, the relationships The homology of apical structures across acetabulate orders is among the Phyllobothriidea, Onchoproteocephalidea, residual also now apparent. This feature appears to have arisen in the ‘‘Tetraphyllidea,’’ and a clade comprising the Cyclophyllidea, common ancestor of the Litobothriidea and the acetabulate clade, Tetrabothriidea, Nippotaeniidea, and Mesocestoides require and to have been lost in the Cathetocephalidea (Fig. 3). Thus, the further investigation. Members of the latter clade parasitize rostellum of cyclophyllideans and some onchoproteocephali- mammals and birds (and teleosts in the case of the few known deans, the apical organ of lecanicephalideans, and the myzorhyn- nippotaeniid species); the majority of hosts are terrestrial. Yet, chus of rhinebothriideans such as Echeneibothrium are Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014) homologous. In many rhinebothriideans, phyllobothriideans, provided evidence that an elasmobranch-hosted genus (e.g., and onchoproteocephalideans, this organ degenerates in the Carpobothrium) is the likely sister taxon to the clade, suggesting transformation to the adult form. But, its presence in the larval that cestode associations with terrestrial hosts (and mammals and stages of many of these is well documented (see Jensen and birds in particular) are derived from elasmobranch-hosted marine Bullard, 2010). ancestors. Clearly, more dense taxon sampling and additional Although hooks occur across cestodes, when interpreted in a markers are required to resolve these relationships more fully. phylogenetic framework it is now apparent that they are not Nonetheless, there can be no doubt that the tapeworms of necessarily homologous across orders. This result allows elasmobranchs are foundational elements of cestode evolution. interpretation of hook composition data we generated years ago, but which were difficult to understand in the context of cestode interrelationships accepted at that time. Among elas- KEY MORPHOLOGICAL FEATURES mobranch cestodes, armature is seen on the apex of the scolex of Historically, the scolex of cestodes has been characterized as some diphyllideans, on the tentacles of trypanorhynchs, as well bearing bothria, bothridia, or suckers, with the latter 2 terms as on some of the bothridiate onchoproteocephalideans and 3 often being used synonymously with acetabula. However, the clades of ‘‘tetraphyllideans’’ (i.e., Calliobothrium species, Mega- fundamental distinction among these structures has often been lonchos species, and the clade containing Pedibothrium and its overlooked in the presence of other distractingly complex features relatives). Hooks are also seen on the rostellum of many of the scolex such as apical organs or the rhyncheal apparatus. As cyclophyllideans and on the bothria of a few bothriocephali- a consequence, the term bothridium has often been casually deans. When armature is mapped onto the phylogenetic tree applied without consideration of structure, even within the past presented by Caira, Jensen, Waeschenbach, Olson, and Little- few decades, for example as was done by Campbell and Beveridge wood (2014) (Fig. 3), it appears that hooks may have evolved (1994) and Khalil (1994) in their treatments of the trypano- independently on at least 8 occasions. The non-homology of rhynchs and diphyllideans, respectively. In 1999, Caira and armature across cestodes is supported by our data on the amino acid composition of hooks. Early work on cyclophyllidean colleagues undertook a comprehensive morphological analysis hooks (e.g., Gallagher, 1964; Dvorak, 1969) showed them to be across cestode orders and resurrected the distinction between comprised of a keratin-like protein, signaled by a relatively high bothria and bothridia made previously by authors such as cystine content. The amino acid profile we generated for the Fuhrmann (1931). They reiterated that although acetabula, a hooks of a replicate cyclophyllidean species (i.e., Taenia term they defined as encompassing both bothridia and suckers, pisiformis) was very much like that reported by Gallagher are membrane-bounded structures consisting of radial muscle (1964) for Echinococcus granulosus (Fig.4A)andalsothat fibers extending between the tegument and the bounding reported by Dvorak (1969) for Taenia taeniaeformis.Analysisof membrane, bothria entirely lack this configuration. They noted the amino acid composition of the hooks of exemplars of 6 of the that unlike the scoleces of the Lecanicephalidea and ‘‘Tetraphyl- other 7 hooked cestode groups (Fig. 4B-L) points to remarkable lidea’’ which bear acetabula in the form of bothridia or suckers, compositional similarities within lineages but substantial differ- those of the Diphyllidea and Trypanorhyncha bear bothria. The ences among lineages. In all cases, the non-cyclophyllidean ubiquity of bothria across trypanorhynchs was later confirmed by lineages exhibited amino acid profiles indicative of proteins Jones et al. (2004) and across diphyllideans by Tyler (2006). This other than keratin, but these proteins have yet to be identified. distinction was of key importance for it brought to light a The hooks of trypanorhynchs are particularly intriguing for fundamental plesiomorphic morphological similarity between the both species analyzed exhibited amino acid profiles that were Trypanorhyncha and Diphyllidea, and other bothriate orders remarkably high in histidine (i.e., 59–70.6% of total amino such as the Diphyllobothriidea and Bothriocephalidea (then acids). It seems likely that the hook proteins exhibited by some collectively referred to as the Pseudophyllidea). Simultaneously, groups (e.g. trypanorhynchs) may be novel and thus represent it revealed the potentially synapomorphic nature of acetabula for particularly fruitful areas for further investigation. a clade of other orders. Molecular support for this notion Scanning electron microscopy across the class has confirmed abounds (e.g., Olson et al., 2001; Waeschenbach et al., 2007, microtriches as a synapomorphy for cestodes (see Chervy, 2009 2012), and the presence of acetabula is now considered a and references therein). Happily, cestodologists have now reached synapomorphy for the immense clade consisting of the majority consensus regarding a standardized terminology for the various of other cestode taxa, including Lecanicephalidea, Rhinebothrii- forms of these unique tegumental extensions, distinguishing a dea, Phyllobothriidea, Onchoproteocephalidea, Cyclophyllidea, small type, referred to as a filithrix, from a large type, referred to Tetrabothriidea, and the residual tetraphyllideans (Caira, Jensen, as a spinithrix. In total, 3 forms of filitriches and 25 forms of Waeschenbach, Olson, and Littlewood, 2014). The lack of spinitriches are recognized. Microthrix form and terminology CAIRA AND JENSEN—ELASMOBRANCH TAPEWORM DIGEST 381

FIGURE 4. Amino acid profiles for hooks of 12 cestode species. Data for 17 common amino acids are presented as percent of total amino acid composition; all samples except those in A and B are from adult specimens. (A) Cyclophyllidea: rostellar hooks from hydatid cysts of Echinococcus granulosus from Gallagher (1964). (B) Cyclophyllidea: rostellar hooks from cysticerci of Taenia pisiformis ex Sylvilagus floridanus. (C) Diphyllidea: apical hooks of Echinobothrium bonasum ex Rhinoptera bonasum. (D) Bothriocephalida: bothrial hooks of Triaenophorus crassus ex Esox lucius. (E) Trypanorhyncha: tentacular hooks of Diplotobothrium springeri ex Sphyrna mokarran. (F) Trypanorhyncha: tentacular hooks of Paragrillotia similis ex Ginglymostoma cirratum. (G) ‘‘Tetraphyllidea’’: bothridial hooks of Calliobothrium violae ex Mustelus canis. (H). ‘‘Tetraphyllidea’’: bothridial hooks of Calliobothrium cf. verticillatum ex Mustelus canis. (I) ‘‘Tetraphyllidea’’: bothridial hooks of Pedibothrium brevispine ex Ginglymostoma cirratum. (J) ‘‘Tetraphyllidea’’: bothridial hooks of Pedibothrium manteri ex Ginglymostoma cirratum. (K) Onchoproteocephalidea: bothridial hooks of Phoreiobothrium cf. lasium ex Prionace glauca. (L) Onchoproteocephalidea: bothridial hooks of Platybothrium auriculatum ex Prionace glauca.

across cestode groups was reviewed by Chervy (2009). It is GENERAL HOST ASSOCIATIONS interesting that much of the substantial variation seen in With only a few exceptions (e.g., Kennedy, 1965), adult cestodes spinitriches occurs among the tapeworms of elasmobranchs; they parasitize vertebrates. Given the unresolved nature of the base of collectively exhibit 21 of the 25 spinithrix forms recognized. the cestode tree, determination of the vertebrate group first Members of the Trypanorhyncha, Diphyllidea, Lecanicephalidea, parasitized is not currently possible. What is clear, however, is and a subset of the Phyllobothriidea are particularly spectacularly that elasmobranchs, once parasitized, served as the source of ornamented. essentially all acetabulate taxa that subsequently went on to 382 THE JOURNAL OF PARASITOLOGY, VOL. 100, NO. 4, AUGUST 2014 parasitize freshwater or terrestrial hosts. Furthermore, it appears specimens of Gollum attenuatus from New Zealand yielded no this may have happened on as few as only 2 occasions. Within the tapeworms. From the standpoint of species coverage, by far the Onchoproteocephalidea, taxa previously referred to the order most poorly known faunas are those of all 3 families of skates and Proteocephalidea, which collectively parasitize a diversity of the catsharks (‘‘Scyliorhinidae’’; shown to be non-monophyletic by freshwater teleosts, a few turtles, and some members of terrestrial Naylor, Caira, Jensen, Rosana, Straube, and Lakner, 2012). groups such as lizards, snakes, and an opossum (see Caneda- Although elasmobranchs are primarily marine, and as a Guzman et al., 2001), appear to represent a monophyletic group consequence, so too are their cestodes, some have the ability to with respect to the members of the order that parasitize batoids of enter estuarine waters, and several groups have made independent euryhaline or even freshwater habitats (see Caira, Jensen, incursions into truly freshwater environments. Notable among Waeschenbach, Olson, and Littlewood, 2014). The second instance these is the Potamotrygonidae, all members of which are endemic involves the well-supported clade containing the Tetrabothriidea, to rivers of South America. Other freshwater elasmobranchs Nippotaeniidea, Mesocestoides, and the remarkably speciose belong to genera that are entirely freshwater (e.g., Glyphis), or Cyclophyllidea. This clade is often referred to as the ‘‘terrestrial predominantly freshwater (e.g., Pristis), or that are otherwise clade’’ because the majority of its members parasitize terrestrial entirely marine (e.g., Dasyatis and Himantura). Work on the birds, mammals, and snakes, with only a few hosted by marine cestodes of potamotrygonids was pioneered by Brooks and his birds and mammals, and freshwater fishes. While the specific collaborators (e.g., Brooks et al., 1981; Mayes et al., 1981) and elasmobranch-hosted taxon that is sister to the ‘‘terrestrial’’ clade is has expanded to include all major river basins (e.g., Marques et unclear, all of the likely candidates given the topologies of the al., 2003; Luchetti et al., 2008; Menoret and Ivanov, 2009; Reyda Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014) trees and Marques, 2011). Cestodes have also been reported from (e.g., Carpobothrium, their New genus 9, Caulobothrium, Dinoboth- Pristis pristis (as P. perotteti) in Lake Nicaragua (e.g., Watson rium þ Ceratobothrium, Pedibothrium and its relatives) are parasites and Thorson, 1976) and from Himantura polylepis (as H. of elasmobranchs, and with the exception of New genus 9, are all chaophraya) in the Kinabatangan River in Borneo (e.g., Fyler parasites of sharks. With respect to the marine members of that and Caira, 2006; Healy, 2006b). Much remains to be learned clade, Hoberg (1995, 1996) has made a strong case that ‘‘terrestrial’’ about cestodes of freshwater sharks and batoids. presence of tetrabothriideans in marine hosts is the result of 1 or Many cestode genera and even some cestode orders are restricted possibly more colonization events involving marine taxa. to elasmobranch orders, families, or in some cases genera. The challenge is to determine which level applies to which cestode ASSOCIATIONS WITH ELASMOBRANCHS group. These associations are most well illustrated at the level of cestode genus because generic monophyly has been the focus of a Our understanding of diversity and interrelationships within substantial amount of recent revisionary systematic work. The the Elasmobranchii has improved substantially over the past 20 following examples illustrate this point. With respect to host genus yr. Over that time, approximately 300 elasmobranch species have fidelity, the lecanicephalidean Eniochobothrium parasitizes only been resurrected or described (White and Last, 2012), bringing the cownose rays of the genus Rhinoptera (see Jensen, 2005) and the known number of species in the subclass to approximately 1,200. ‘‘tetraphyllidean’’ Yorkeria parasitizes only bamboo sharks of the The first comprehensive molecular phylogeny, generated using a genus Chiloscyllium (see Caira et al., 2007). With respect to host single gene approach, is now available (Naylor, Caira, Jensen, family fidelity, the lecanicephalidean Tetragonocephalum parasitizes Rosana, Straube, and Lakner, 2012). This work is being only stingrays of the family Dasyatidae (see Jensen, 2005) and the significantly expanded upon by inclusion of additional markers onchoproteocephalidean Platybothrium parasitizes only sharks of and taxa with support from NSF’s AToL program (G. Naylor, the family Carcharhinidae (see Healy, 2003). The cathetocephali- pers. comm.). The Naylor, Caira, Jensen, Rosana, Straube, and dean Cathetocephalus is also restricted to this host family (Caira et Lakner (2012) tree provides support for the mutual monophyly of al., 2005). Litobothrium parasitizes only 3 of the 7 families of 2 major groups of elasmobranchs, the batoids (i.e., stingrays and lamniform sharks; as it is the only genus in its order, the order their relatives) and the selachians (i.e., sharks). At present 12 Litobothriidea is thus also restricted to these families (Olson and orders (4 batoid and 8 shark), 54 families (20 batoid and 34 Caira, 2001). The significance of understanding these affiliations is shark), and 195 genera (89 batoid and 106 shark) of elasmo- that once the nature and level of host associations have been branchs are recognized (Ebert et al., 2013). determined, robust predictions about the cestode faunas of host Within elasmobranchs, the tapeworm faunas of near-shore, taxa not yet examined can be made. shallow-water taxa are most well studied. However, tapeworms At the species level, specificity is usually much tighter. For the have been reported from all 12 elasmobranch orders. At least 1 most part, cestodes of elasmobranchs exhibit oioxenous (i.e., species in all 20 batoid families has been examined for, and found species-specific) associations with their hosts. This has been to host, cestodes. Among sharks, at least 1 species in 28 of the 34 observed in onchoproteocephalideans (e.g., Caira and Jensen, families has been examined for cestodes, but the faunas of the 2001, 2009; Fyler et al., 2009), diphyllideans (Tyler, 2006; Caira, Proscylliidae, Pseudocarchariidae, Rhincodontidae, Oxynotidae, Marques et al., 2013), litobothriideans (Olson and Caira, 2001), Echinorhinidae, and Chlamydoselachidae are completely un- cathetocephalideans (Caira et al., 2005), rhinebothriideans known. All but 2 of the 28 shark families examined are known (Healy, 2006a), lecanicephalideans (Jensen, 2005), phyllobo- to host cestodes. The exceptions are the Leptochariidae and thriideans (Ruhnke, 2011), and ‘‘tetraphyllideans’’ (e.g., Caira et Pseudotriakidae. Neither group is particularly speciose; the former al., 2004, 2007); in many of these instances confirmation has is monotypic and the latter includes only 4 species in 3 genera. been provided using molecular data. The situation in trypano- Examination of 34 specimens of Leptocharias smithii off Senegal, 3 rhynchs diverges from this pattern. The assessment of host specimens of Pseudotriakis microdon from the Azores, and 6 specificity by Palm and Caira (2008) using the Host Specificity CAIRA AND JENSEN—ELASMOBRANCH TAPEWORM DIGEST 383

index (HSs) of Caira et al. (2003) yielded a mean index value of much larger role teleosts play in the life cycles of many of these 3.86 for the 63 species of adult trypanorhynchs examined, as taxa than suspected. The key to larval types provided by Jensen compared to a value of 0 for the oioxenous taxa typical of the and Bullard (2010), which was generated using both morpho- other orders (Caira et al., 2003). As specific examples, Grillotia logical and molecular data, provides guidance for future such erinaceus has been reported from several orders of batoids and work. sharks, as has Lacistorhynchus dollfusi (seePalm,2004).Thus, Longevity of tapeworms in elasmobranchs has yet to be for a reason that is not yet understood, host specificity in the assessed with certainty. Existing indirect evidence suggests they Trypanorhyncha appears to be more relaxed than it is in any of are much shorter lived than cestodes that parasitize mammals, the other elasmobranch-hosted orders. As a consequence, which are considered to live for up to decades (e.g., Read, 1967; trypanorhynch specificity at categories of classification above Roberts et al., 2013). Evidence comes from seasonal studies species also appears to be more relaxed and thus also less involving large sample sizes, such as those of McCullough et al. predictable. (1986) and Pickering and Caira (2014), in which prevalence and intensity of infections of cestodes parasitizing Squalus acanthias LIFE CYCLES declined sharply at certain times of the year, which is consistent with the death of worms on an annual basis. Work examining The life cycles of elasmobranch tapeworms are particularly cestode faunal compositions in individuals of the stingray poorly known, a fact that is reiterated each time the subject has Dasyatis americana of different ages (T. Mattis, pers. comm., in been raised (e.g., Chambers et al., 2000; Chervy, 2002; Palm, Caira, 1990), showing that faunas turn over, rather than expand 2004; Caira and Reyda, 2005; Jensen, 2005; Jensen and Bullard, over time, supports individual worm longevity of several years at 2010). A complete life cycle has yet to be established for even a most. single species in nature, although Sakanari and Moser (1989) completed the life cycle of the trypanorhynch Lacistorhynchus GEOGRAPHICAL DISTRIBUTION dollfusi experimentally. It is generally thought that elasmo- branch cestodes parasitize 2 or perhaps 3 different intermediate Given that tapeworms are ubiquitous residents of the spiral host species before their elasmobranch definitive host. The intestine of elasmobranchs and elasmobranchs are found around existence of a fourth intermediate, or possibly paratenic, host the globe, it is not unexpected that their tapeworms are also has been suggested in some cases (e.g., Palm, 2004). Life cycle global in distribution. Elasmobranch cestodes from the coastal stages are trophically transmitted between hosts in the life cycle waters off Europe (e.g., Rudolphi, 1819; van Beneden, 1850; sequence. Taxa serving as intermediate or possibly paratenic Dollfus, 1942; Williams, 1959) and North America (e.g., Linton, hosts in the marine environment were summarized by Caira and 1889, 1890, 1908, 1924) were among the first documented. Reyda (2005). Life cycle work is severely hampered by the Cestodes are now known from elasmobranchs in all major ocean difficulties associated with identifying cestode larvae to species, basins and Antarctic (e.g., Wojciechowska, 1990) and arctic (J. or in some cases even to higher taxon level. The notable Caira, pers. obs.) waters. They have been reported from the exception is the Trypanorhyncha. The presence of a fully armed Mediterranean Sea (e.g., Euzet, 1959), Black Sea (Vasileva et al., rhyncheal apparatus, which is diagnostic at the species level, 2002), Baltic Sea (Rudolphi, 1819), North Sea (e.g., McVicar, allows for identification of trypanorhynch larvae to species in 1976), Red Sea (e.g., Ramadan, 1984), Persian Gulf (e.g., Malek intermediate hosts, be they teleosts, molluscs, crustaceans, et al., 2010), Gulf of Mexico (e.g., Jensen, 2009), and Gulf of jellyfishes, or sea cucumbers (see Palm, 2004). In contrast, the Thailand (e.g., Caira and Tracy, 2002). There are records from literature is rife with reports of cestode larvae that lack the waters surrounding oceanic islands such as Taiwan (e.g., Fyler, rhyncheal apparatus and thus are of unknown or uncertain 2011), New Caledonia (e.g., Beveridge and Justine, 2010), identity, from a wide array of marine animals (see Dollfus, 1976; Kiribati (Richmond and Caira, 1991), Galapagos Islands (Nock Chambers et al., 2000; Caira and Reyda, 2005; Jensen and and Caira, 1988), Solomon Islands (Cielocha et al., 2013), the Bullard, 2010, and references therein). Recent applications of Azores (e.g., Noever et al., 2010; Caira and Pickering, 2013), molecular methods have substantially improved the situation, Japan (e.g., Yamaguti, 1934, 1952), as well as larger islands such for they have allowed morphologically amorphous or divergent as Iceland (e.g., Beveridge and Campbell, 2007), Greenland larval forms to be associated with their adult counterparts. (Baer, 1956), and New Zealand (e.g., Robinson, 1959). Some of Much of this work has focused on specific larval types found in the most well characterized elasmobranch cestode faunas are squid (e.g., Brickle et al., 2001; Randhawa and Brickle, 2011), now those of Australia (e.g., Campbell and Beveridge, 2002; cetaceans (e.g., Agusti et al., 2005; Aznar et al., 2007; Beveridge and Campbell, 2005; Ruhnke, Healy, and Shapero, Randhawa, 2011), the cephalochordate Amphioxus (Holland et 2006; Caira et al., 2007; Cielocha and Jensen, 2013), the Gulf of al., 2009), and bivalves (e.g., Holland and Wilson, 2009). A more California (e.g., Jensen, 2001; Tyler, 2001; Ghoshroy and Caira, comprehensive approach was taken by Jensen and Bullard 2001; Campbell and Beveridge, 2006), and Borneo (e.g., Ruhnke, (2010) who generated partial (i.e., D1-D3) 28S ribosomal DNA Caira, and Carpenter, 2006; Koch et al., 2011; Schaeffner et al., sequence data for 25 species of adult cestodes from elasmo- 2011). With respect to South America, records exist from both branchs and 27 larval cestode species from teleosts, molluscs, the western coast (e.g., Carvajal and Dailey, 1975; Campbell and and shrimps in the Gulf of Mexico. Their work led to the Carvajal, 1987) and eastern coast (e.g., Ivanov and Campbell, identification of specific larval forms that could be confidently 2002; Ivanov and Brooks, 2002). In addition, as noted above, assigned to rhinebothriidean, ‘‘tetraphyllidean,’’ and also what cestodes are known from elasmobranchs in all of the major river are now recognized as phyllobothriidean and onchoproteoce- basins of South America, several rivers of Borneo, and Lake phalidean genera. Among other inroads, their work revealed the Nicaragua. 384 THE JOURNAL OF PARASITOLOGY, VOL. 100, NO. 4, AUGUST 2014

With the exception of a few records from South Africa (e.g., By far the most depauperate faunas are those of deeper water Palm, 1999; Caira, Rodriguez, and Pickering, 2013), Madagascar sharks (e.g., Caira and Pickering, 2013). At this point it is not (e.g., Caira and Rasolofonirina, 1998; Jensen and Caira, 2008), entirely clear whether there is a phylogenetic component to this and Senegal (e.g., Caira, Rodriguez, and Pickering, 2013; Jensen phenomenon, for the majority of deeper water sharks belong et al., In Press), data on elasmobranch cestodes from the coasts of either to the order Squaliformes (dogfish sharks) or the many African countries are extremely limited. But, by far the carcharhiniform family ‘‘Scyliorhinidae’’ (catsharks). Nonethe- most problematic regions of the world are the coastal waters less, both prevalence and intensity of infection is extremely low, surrounding India and Sri Lanka. The reasons for this are two- and these elasmobranchs typically harbor infections that consist fold. First, some of the earliest comprehensive work on of only a single species of tapeworm. elasmobranch cestodes was conducted off Sri Lanka (then Ceylon) (e.g., Shipley and Hornell, 1905, 1906; Southwell, 1911, TRACKING ELASMOBRANCH HOSTS AND IDENTITIES 1912, 1925, 1929, 1930a, 1930b) in conjunction with the British- funded pearl oyster industry. Although the majority of the The fact that more than 300 elasmobranch species have been descriptions in these works are reasonably detailed and well described or resurrected over the past 20 yr underscores the illustrated, it is often difficult to place them into modern importance of verifying the identities of elasmobranch specimens taxonomic schemes, and unfortunately, much of the type material from which tapeworms are collected. As many of the more associated with these works is missing. Shipley and Hornell’s taxonomically problematic elasmobranchs belong to common material is lost and although some of Southwell’s specimens are genera that were among the first reported to host tapeworms, they deposited at the Natural History Museum in London, that is not challenge many historical host records. Such genera include, for the case for most of his material. However, the work of example, Squalus (see Last et al., 2007), Aetobatus (see White et Subhapradha (e.g., 1955) aside, of even greater concern is the al., 2010), and Pastinachus (see Last and Manjaji-Matsumoto, substantial number of problematic, very superficial and poorly 2010). In many cases, confirmation of host associations requires illustrated descriptions of elasmobranch tapeworms that have collection of new cestode material from hosts of verified identity. come from India in the last approximately 40 yr. Of the more than Moving forward, a standard method for documenting elasmo- 150 species described from that region since 1979, almost 30% branch host identities must be used. In collaboration with have already been determined to be species inquirenda, nomina elasmobranch biologists, we have developed a DNA-based nuda, or synonyms; the remainder has yet to be verified. Host approach for verifying elasmobranch species identities that has identifications for most species are questionable, even at the genus involved generation of sequence data for approximately 1,000 level. What is even more problematic is the complete lack of type base pairs of the mitochondrial protein-coding gene NADH material of these species available for study. Recollection of dehydrogenase subunit 2 (NADH2; see Naylor, Caira, Jensen, essentially all species will be needed to rectify this situation. Rosana, Straube, and Lakner, 2012; Naylor, Caira, Jensen, Rosana, White, and Last, 2012; Straub et al., 2013) for multiple CESTODE ASSEMBLAGES individuals representing more than 575 verified elasmobranch species across the Elasmobranchii, many of which were sampled Cestodes comprise by far the majority of the fauna parasitizing for cestodes. Reference sequence data for this gene for these the spiral intestine of most elasmobranch taxa (e.g., Cislo and species are now available in GenBank (see Naylor, Caira, Jensen, Caira, 1993; Curran and Caira, 1995), with nematodes, in addition Rosana, Straube, and Lakner, 2012; Naylor, Caira, Jensen, to the occasional digenean, acanthocephalan, and rarely monoge- Rosana, White, and Last, 2012). A small sample of liver or muscle nean occurring in some (Caira et al., 2012). Examination of the tissue is now routinely collected from all host specimens examined spiral intestine of any elasmobranch anywhere in the world is likely and NADH2 data are generated and compared to this library for to yield cestodes, for they are essentially ubiquitous. Cestode confirmation of specific identity. Work towards generating and infections can range from a single to thousands of individuals in a depositing NADH2 sequence data for all elasmobranch species single host specimen. Cestode faunal complexity varies widely continues. As a consequence, the GenBank library continues to across elasmobranch groups. By far the most complex and diverse expand. To corroborate molecular-based identifications, we have cestode assemblages are seen in batoids, and in particular in species established a publicly available on-line database for housing of Dasyatidae (stingrays) and Myliobatidae (eagle rays). The co- images and data for each host specimen examined occurrence of multiple congeners, several genera in the same order, (elasmobranchs.tapewormdb.uconn.edu). In the field, each host and representatives of several orders is common in even a single specimen is assigned a unique combination of Collection Code host individual. For example, the eagle ray Aetobatus ocellatus may and Collection Number (e.g., BO-11) and a series of digital host as many as 28 species of cestodes (White et al., 2010; Mojica et photographs is taken along with basic morphometric data. Once al., 2014) representing what are now recognized as 5 orders and 19 uploaded to the database, this unique record allows each host genera of tapeworms. Admittedly, in the past, issues with specimen and its associated cestodes (and other parasites) to be misidentification of congeneric hosts involving morphologically easily tracked, while facilitating comparisons of data and images similar or even cryptic species have plagued assessments of host across host specimens. Although labor-intensive, we urge future specificity and concomitantly determinations of cestode assemblage workers to consider following this protocol for all elasmobranch diversity (e.g., Fyler and Caira, 2010). As efforts to resolve and specimens serving as hosts, for the benefits in terms of accuracy stabilize elasmobranch taxonomy continue (White and Last, 2012), and longevity/stability of host identifications cannot be overem- the issue of host identification is becoming more tractable, phasized. We note that others have generated cytochrome c particularly if the protocol for host tracking outlined below oxidase subunit I (COI) data to employ a DNA-barcoding becomes more widely adopted. approach to recognize species boundaries in elasmobranchs (e.g., CAIRA AND JENSEN—ELASMOBRANCH TAPEWORM DIGEST 385

Ward et al., 2008); however, the reference library for NADH2 is intercalate their scolex into existing elements of the mucosa (e.g., more extensive and includes more vouchered (either with McKenzie and Caira, 1998) and those that physically transform photographs or museum specimens) elasmobranch species. the mucosa into a configuration that allows them to attach more effectively (e.g., Borucinska and Caira, 1993; Caira, Jensen, OTHER CONSIDERATIONS Waeschenbach, and Littlewood, 2014). Furthermore, site of attachment within the spiral intestine has been characterized Although studies documenting and describing parasite and host either for entire cestode faunas (e.g., Cislo and Caira, 1993; diversity and phylogenetic relationships dominate the elasmo- Curran and Caira, 1995), or subsets of species comprising faunas branch-tapeworm literature, other aspects of this system have (e.g., Williams et al., 1970; McVicar, 1979; Randhawa and Burt, been explored. These other areas are highlighted below, focusing 2008; Twohig et al., 2008). This work was often conducted in on more recent work. However, we would be remiss in this review concert with investigations of mode of attachment. if we did not mention the wonderfully detailed works of Rees and Studies examining the physiological basis of this host-parasite Williams (e.g., Rees, 1941, 1946, 1959, 1961; Rees and Williams, system do not date beyond those of early workers such as Read 1965; Williams, 1966) that have contributed substantially to our (1957), Simmons et al. (1960), and Pappas and Read (1972). This understanding of the functional morphology of a variety of is unfortunate for we believe much is to be gained from applying elasmobranch cestodes. more modern methods to characterize the physiology of the spiral Ultrastructural investigations of elasmobranch tapeworms intestine and the absorption of nutrients across the cestode using transmission electron microscopy have elucidated details tegument, especially as these might relate to attachment site of scolex and strobilar morphology and anatomy. The central specificity. nervous system has been characterized in trypanorhynchs Given the complexity of cestode faunas in elasmobranchs and (Biserova, 2008; Biserova and Korneva, 2012). Ultrastructural the relative difficulty in obtaining samples and thus appropriate elements of spermiogenesis and/or spermatozoa are among the sample sizes, ecological aspects of this host-parasite system have most well studied features; this body of work was reviewed by been given relatively little consideration compared to freshwater Levron et al. (2010). Most recently, work has focused on and terrestrial host-parasite systems. Much of the ecological work diphyllideans (Marigo et al., 2011a), lecanicephalideans (Cielocha has focused on characterization of communities and potential et al., 2013), onchoproteocephalideans (Marigo et al., 2011b), but mainly trypanorhynchs (Miquel and S´widerski, 2006; Miquel et competition, specifically whether the assemblages interact (e.g., al., 2007; Marigo, S´widerski et al., 2011). Similarly, ultrastruc- Kennedy and Williams, 1989; Cislo and Caira, 1993; Curran and tural detail of vitellogenesis has been studied in diphyllideans Caira, 1995; Friggens and Brown, 2005; Alarcos et al., 2006; (S´widerksi et al., 2011) and some trypanorhynchs (S´widerski et Keeney and Poulin, 2007; Randhawa, 2012). Elasmobranch al., 2006a, 2006b, 2012). Regions of the scolex of diphyllideans parasite assemblages have also been used to identify diversity (Biserova, 1992), ‘‘tetraphyllideans’’ (McCullough and Fair- hotspots (Poulin et al., 2011). Seasonality of infection has been weather, 1989), and trypanorhynchs (Jones and Beveridge, explored (McCullough et al., 1986; Pickering and Caira, 2014), as 1998) have also been characterized, as has the terminal genitalia has the relationship between host and cestode body size of a phyllobothriidean (Beveridge and Smith, 1985). (Randhawa and Poulin, 2009, 2010a), and species richness in Although cestodes are not known to cause substantial damage relation to environmental factors and host phylogeny (Randhawa to their hosts, several studies have documented the pathological and Poulin, 2010b). The potential of elasmobranch parasites for responses at the site of attachment to the mucosal of the spiral use as biological tags was reviewed by Caira (1990); Moore (2001) intestine. Cestodes involved have included trypanorhynchs (e.g., and Yamaguchi et al. (2003) conducted detailed field studies Borucinska and Caira, 1993, 2006; Borucinska and Dunham, exploring this potential in sharks off Great Britain and Japan, 2000), ‘‘tetraphyllideans’’ (Borucinska and Caira, 1993), and respectively. lecanicephalideans (Borucinska et al., 2013). In addition, larval Surprisingly little work has been done exploring the coevolu- trypanorhynchs have been associated with histopathological tionary relationships between cestodes and their elasmobranch changes at the site of their attachment to the liver of sharks hosts. This is in large part because robust phylogenies for (Campbell and Callahan, 1998; Cousin et al., 2003) and with elasmobranchs and their cestodes have been lacking. To our lesions in the gastric wall of a cownose ray (Borucinska and knowledge, the only published study comparing phylogenetic Bullard, 2011). trees generated independently for both taxa was that of Caira A relatively large body of work exists characterizing the mode and Jensen (2001) who used trees for hosts and parasite of attachment of cestodes to the intestinal mucosa. This work counterparts that were extremely preliminary. The pattern seen has included exemplars of all 9 orders: cathetocephalideans (e.g., revealed a substantially greater amount of discordance than Caira et al., 2005), diphyllideans (e.g., Twohig et al., 2008), expected given the high degree of host specificity of the cestode trypanorhynchs (e.g., Borucinska and Caira, 1993, 2006), taxa included. Documentation of the degree of coevolution in lecanicephalideans (e.g., Jensen et al., 2011; Borucinska et al., most of the elasmobranch cestode groups and ultimately the 2013; Jensen and Russell, 2014), litobothriideans (e.g., Dailey, processes underlying these patterns remains 1 of the most 1969; Caira, Jensen, Waeschenbach, and Littlewood, 2014), exciting and potentially productive areas of investigation in this onchoproteocephalideans (e.g., McVicar, 1972; Williams, system. As robust and extensive species-level phylogenies for 1968a), phyllobothriideans (e.g., Williams, 1968b; McKenzie elasmobranchs (e.g., Naylor, Caira, Jensen, Rosana, Straube, and Caira, 1998), rhinebothriideans (e.g., Williams et al., 1970), and Lakner, 2012) and cestodes (e.g., Fyler, 2009; Healy et al., and ‘‘tetraphyllideans’’ (e.g., Williams et al., 2004). In general, a 2009; Palm et al., 2009; Olson et al., 2010; Caira, Jensen, distinction can be made between species that either grasp or Waeschenbach, Olson, and Littlewood, 2014) become more 386 THE JOURNAL OF PARASITOLOGY, VOL. 100, NO. 4, AUGUST 2014 available, we anticipate that interest in these questions will infecting the spiral intestine of the nurse shark, Ginglymostoma blossom. cirratum. Journal of Parasitology 79: 238–246. ———, AND ———. 2006. Mode of attachment and lesions associated Tapeworms and their elasmobranch hosts now constitute 1 of with trypanorhynch cestodes in the gastrointestinal tracts of two the most well-documented host-parasite systems known. As a species of sharks collected from coastal waters of Borneo. Journal of consequence, this system is now poised to serve as the focus of Fish Diseases 29: 395–407. intensive studies aimed at understanding the fundamental ———, AND A. DUNHAM. 2000. Lesions associated with attachment of the cestode Tentacularia sp. to the duodeno-spiral junction in the blue principles of parasite ecology, evolution, and host associations. shark, Prionace glauca (L.), with a description of the intestinal It is our hope that the synthesis provided here will serve to pave morphology of the shark. Journal of Fish Diseases 23: 353–359. the way for future such studies. ———, J. J. CIELOCHA, AND K. JENSEN. 2013. 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