A digest of elasmobranch tapeworms.

A Digest of Elasmobranch Tapeworms Author(s): Janine N. Caira and Kirsten Jensen Source: Journal of Parasitology, 100(4):373-391. 2014. Published By: American Society of Parasitologists DOI: http://dx.doi.org/10.1645/14-516.1 URL: http://www.bioone.org/doi/full/10.1645/14-516.1

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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 speciesspecific (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.

suckers. Cestode orders vary in diversity from fewer than 10 to hundreds of species (Fig. 2). All but the ‘‘Tetraphyllidea’’ are almost certainly monophyletic. With a few exceptions, elasmobranch tapeworms are moderate in size relative to other cestode groups, with most species ranging in length from 500 lm to 60 cm. Members of some orders exclusively parasitize sharks, others exclusively batoids, and some parasitize both groups. Almost all reside in the spiral intestine of their hosts. The majority of species occupy marine environments; the exception is the Onchoproteocephalidea as only a subset parasitizes elasmobranchs and many occur in freshwater. In all but the Trypanorhyncha, host fidelity at the species level is usually strict. For context and because the taxonomy and systematics of these groups has been moving forward so rapidly, a brief synopsis of each of the 9 orders as they are currently configured is provided below.

The tapeworms that parasitize elasmobranchs (i.e., sharks and rays) exhibit a spectacular variety of forms (Fig. 1A-J). Interpretations of the relationships underlying these forms have varied substantially and have manifested in divergent higher classification schemes. For example, Schmidt (1986) recognized 6 orders (Dioecotaeniidea, Litobothriidea, Diphyllidea, Lecanicephalidea, Tetraphyllidea, Trypanorhyncha), but Khalil et al. (1994) recognized only the latter 4 orders. Historically, there has been a tendency to group cestodes exhibiting these relatively disparate morphological forms together in higher-level classifications, perhaps in part because of their shared associations with elasmobranchs. However, over the past 2 decades, substantial inroads have been made in our understanding of the evolution, classification, and host associations of these parasites. In total, 977 species and 201 genera are now recognized; approximately 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 these taxa; instead readers are referred to the Global Cestode Database (www.tapewormdb.uconn.edu) for information on individual species and genera and to Caira et al. (1999) for a detailed treatment of the terminology applied to the morphological features of these groups. Here we review current assessments of the diversity and evolution of tapeworms of elasmobranchs, their host associations, and the key role they have played in the evolution of cestodes overall. Tapeworms of elasmobranchs are now considered to constitute 9 of the 19 cestode orders. With the exception of litobothriideans and cathetocephalideans, they are generally divided into bothriate or acetabulate forms based on scolex morphology; acetabulate forms are further characterized as bearing bothridia or simple

CATHETOCEPHALIDEA Schmidt & Beveridge, 1990 (Fig. 1F) With only 7 valid species and 3 valid genera the Cathetocephalidea is one of the least speciose elasmobranch cestode orders. Its members are characterized by a scolex that lacks bothria or acetabula, and instead consists of an anterior globose or transversely extended region and a posterior rugose base with or without a band of papillae. Species are moderate in size ranging in total length from 3–10 cm. Cathetocephalideans are oioxenous, sensu Euzet and Combes (1980); each species parasitizes a different species of carcharhinid shark, specifically of the genera Carcharhinus and Lamiopsis. Collectively, these records indicate an essentially circumglobal distribution. The order was established by Schmidt and Beveridge (1990) for Cathetocephalus. It was expanded to include Sanguilevator by Caira et al. (2005), and most recently, to also include Disculiceps (see Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014).

* Department of Ecology and Evolutionary Biology and the Biodiversity Institute, University of Kansas, Lawrence, Kansas 66045. DOI: 10.1645/14-516.1 373

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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

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lished by Marques et al. (2012) for weakly armed taxa from catsharks. Caira, Marques et al. (2013) published a reconfiguration of the order, aimed at the circumscription of monophyletic genera, that led to the erection of the additional genera Andocadoncum, Coronocestus, and Halysioncum. 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) diversity of elasmobranch tapeworm orders. Note that more than half of the Onchoproteocephalidea parasitize vertebrates other than elasmobranchs.

The latter study supported a sister taxon relationship between Sanguilevator and Cathetocephalus. The latter 2 genera are housed in the Cathetocephalidae; Disculiceps belongs to the Disculicepitidae. This order is deeply nested among the acetabulate orders of cestodes in the trees of Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014), suggesting its non-acetabulate scolex is a derived condition. The number of carcharhinid species that remain to be examined for cestodes suggests the order is likely much more diverse than current records indicate. DIPHYLLIDEA van Beneden in Carus, 1863 (Fig. 1A) At the time of the Tyler (2006) monograph, this order was considered to consist of only 2 valid genera (i.e., Ditrachybothridium and Echinobothrium). Ahamulina was subsequently estab-

With 116 valid species in 24 valid genera, the Lecanicephalidea is 1 of the more specious orders of elasmobranch tapeworms. The scolex consists of 4 simple bothridia or suckers and, with few exceptions (e.g., Jensen, 2001), an apical structure. The order’s monophyly is supported by morphological (Caira et al., 2001) and molecular (Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014) data. Although a synapomorphy for the Lecanicephalidea is lacking, most species are distinctive in their possession of a vagina that opens into the genital atrium posterior (rather than anterior) to the cirrus sac and a vas deferens that extends from the level of the ovary to the cirrus sac. Lecanicephalideans are generally less than 1 mm, but they range from 400 lm (e.g., Jensen, 2001) to more than 6 cm (e.g., Butler, 1987) in total length. They primarily parasitize batoids, although some records from sharks exist (Caira et al., 1997; Jensen, 2005); all occur in the marine environment. Among batoids, they have been reported from 12 of 23 families and 3 of 4 orders; they are conspicuously absent from Rajiformes. With very few exceptions (e.g., Cielocha et al., 2014), species exhibit oioxenous specificity for their hosts. Generic diversity of lecanicephalideans is greatest in stingrays (Dasyatidae) and eagle rays (Myliobatidae). The order has an affinity for warmer, coastal

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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.’’


waters (i.e., between latitudes of 408N and 408S). It is circumglobal in distribution; diversity is highest in Indo-Pacific waters. With 13 of the 24 genera established since 1995, an updated familial classification based on a robust phylogenetic analysis, with representation beyond the 11 genera included by Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014), is long overdue. Furthermore, ongoing studies of lecanicephalideans, mainly from batoids of Southeast Asia, suggest that species level diversity in the order is substantially underestimated. LITOBOTHRIIDEA Dailey, 1969 (Fig. 1C) This is the second least speciose of elasmobranch-hosted cestode orders. The 9 species in the order are all members of the single genus Litobothrium. The suppression of the second genus, Renyxa, by Euzet (1994) was supported by the molecular analyses of Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014). With 1 notable exception, the litobothriidean scolex consists of an apical sucker followed by a series of pseudosegments, a subset of which is cruciform. The exception is L. aenigmaticum, which beyond its possession of coniform spinitriches, bears absolutely no resemblance to its congeners, and in fact, little resemblance to cestodes because reproductive organs have yet to be found. Nonetheless, molecular data robustly place it among the species in this order (Caira, Jensen, Waeschenbach, and Littlewood, 2014). Typical litobothriideans range in size from approx. 1 to 9 mm; L. aenigmaticum from 14 to 32 mm. Litobothriideans are oioxenous; each species associates with only a single species of lamniform shark. Among lamniforms, they are restricted to Alopiidae (thresher sharks), Mitsukurinidae (goblin shark), and Odontaspididae (sand tiger sharks). As few species in these host families remain to be examined for cestodes, discovery of many additional species seems unlikely. The order was established by Dailey (1969) and is known only from the Pacific Ocean. It is considered to represent the sister taxon to the acetabulate clade of cestodes (Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014) suggesting that its lack of scolex acetabula represents an ancestral condition. ONCHOPROTEOCEPHALIDEA Caira, Jensen, Waeschenbach, Olson & Littlewood, 2014 (Fig. 1H) Representing a combination of taxa previously assigned to the Proteocephalidea and most of those assigned to the ‘‘tetraphyllidean’’ family Onchobothriidae, this is the only cestode order that includes both elasmobranch-hosted genera as well as genera hosted by other vertebrate groups. Despite the somewhat radical nature of recognition of these taxa as members of the same order, support for their common evolutionary history is compelling (e.g., Olson et al., 2001; Caira et al., 2005; Waeschenbach et al., 2007, 2012; Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014). A robust synapomorphy for the order has yet to be identified, but the presence of gladiate spinitriches throughout the length of the strobila is at least a candidate feature (Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014). The order is dominated by genera that parasitize vertebrates other than elasmobranchs (i.e., 71 of 83 genera). In fact, the majority of species parasitize freshwater fishes, but the order also includes

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species that parasitize snakes, amphibians, and even a mammal. We will not treat these species here, and instead refer readers to de Chambrier et al. (2004). The mere 12 genera hosted by elasmobranchs include a disproportionate amount of the diversity in the order (i.e., 213 of 580 species) largely because of the speciose Acanthobothrium with more than 150 members. With the exception of Prosobothrium (see Olson et al., 2001), all 12 genera are characterized by their possession of 1 or 2 pairs of bothridial hooks on each of their 4 bothridia. Species range in size from 1 mm to 15 cm. There is some evidence from molecular analyses (Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014) that the taxa previously assigned to the Proteocephalidea represent a monophyletic group within the Onchoproteocephalidea. This does not appear to be the case for the genera previously assigned to the ‘‘Tetraphyllidea.’’ With a few exceptions (e.g., Healy, 2003), elasmobranch-hosted onchoproteocephalidean species exhibit oioxenous specificity. But they are hosted by an eclectic selection of elasmobranch groups, with an emphasis on carcharhiniform sharks (i.e., the cestode genera Megalonchos, Phoreiobothrium, Platybothrium, Prosobothrium, and Triloculatum) and myliobatiform batoids (i.e., Acanthobothroides, Onchobothrium, Pinguicollum, Potamotrygonocestus and Uncibilocularis). However, New genus 8 of Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014) parasitizes Rhinopristiformes. Of particular note is Acanthobothrium; it is unique among the 110 elasmobranchhosted acetabulate genera in that its species parasitize multiple orders of batoids and sharks. Given that many of the non-hooked members of the order parasitize hosts in freshwaters, it is interesting that the elasmobranch-hosted groups include those found in freshwater elasmobranchs (Potamotrygonocestus) as well as those found in hosts that often occur in euryhaline habitats (e.g., Acanthobothroides and New genus 8). By far the majority of records come from tropical and subtropical waters, but species are known from latitudes above 608N (e.g., Manger, 1972). PHYLLOBOTHRIIDEA Caira, Jensen, Waeschenbach, Olson & Littlewood, 2014 (Fig. 1G) In the not too distant past (e.g., Euzet, 1994), most of the ‘‘tetraphyllidean’’ non-hooked acetabulate genera were assigned, in many cases by default, to the family Phyllobothriidae. The substantial morphological variation seen among this assortment of taxa was accommodated by the subfamily designations Thysanocephalinae, Echeneibothriinae, Phyllobothriinae, Triloculariinae, and Rhinebothriinae. To a large extent, the recent dismantling of the ‘‘Tetraphyllidea’’ (Healy et al., 2009; Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014) has emerged from a series of studies critically evaluating the morphology of genera traditionally assigned to the Phyllobothriidae (e.g., Ruhnke, 1993, 1994, 1996a, 1996b; Ivanov, 2008; Ruhnke and Caira, 2009). But it was also informed by the discovery and description of novel generic forms (e.g., Caira and Durkin, 2006; Ivanov, 2006; Ruhnke, Caira, and Carpenter, 2006; Caira et al., 2011; Ruhnke and Workman, 2013). In establishing the Rhinebothriidea, Healy et al. (2009) removed the Rhinebothriinae and Echeneibothriinae from the Phyllobothriidae. In his monograph, Ruhnke (2011) addressed the polyphyletic nature of the Phyllobothriidae and provided a more restricted concept of the family. In that work, he also determined the taxonomic status

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of essentially all species and genera that have historically been assigned to the family in the context of his revised definition. As a result of their molecular phylogenetic analyses, Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014) elevated the family to ordinal status. With only a few exceptions, the genera assigned to the order were consistent with those assigned to the family by Ruhnke (2011). In general, phyllobothriideans exhibit simple, undivided bothridia each of which bears an apical sucker; some (e.g., Orectolobicestus and Nandocestus) also bear marginal loculi. Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014) considered as many as 24 genera and 72 species to belong to the order. However, as their analyses included representation of only 12 of these genera and apical suckers are seen in other cestode orders (e.g., some Rhinebothriidea) uncertainty remains with respect to membership of the Phyllobothriidea. The majority of taxa parasitize sharks, with an emphasis on Carcharhiniformes (i.e., the cestode genera Alexandercestus, Doliobothrium, Hemipristicola, Orygmatobothrium, Paraorygmatobothrium, Pelichnibothrium, Phyllobothrium, Ruhnkecestus, Scyphophyllidium, Thysanocephalum, and New genus 10 of Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014); but also Pristiophoriformes (i.e., Bib ursibothrium, Cardiobo thriu m, and Flexibothrium); Squaliformes (i.e., Bilocularia and Trilocularia); Orectolobiformes (i.e., Orectolobicestus); and Lamniformes (i.e., Marsupiobothrium). The few members that parasitize batoids are hosted by Myliobatiformes (i.e., Anindobothrium and Nandocestus); Torpediniformes (i.e., Calyptrobothrium); and Rajiformes (i.e., Guidus). The unexpected occurrence of Chimaerocestos in holocephalans is considered to represent a host-capture event (Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014). Collectively, the phyllobothriideans exhibit essentially a cosmopolitan distribution, but records are less common at higher latitudes. RHINEBOTHRIIDEA Healy, Caira, Jensen, Webster & Littlewood, 2009 (Fig. 1E) Exciting progress has been made in the systematics of this group of cestodes in the last few years. Recognition of these taxa in an order independent from the ‘‘Tetraphyllidea’’ was the result of morphological work conducted by Healy (2006a) and molecular analyses presented by Healy et al. (2009). Rhinebothriideans resemble ‘‘tetraphyllideans’’ in their possession of a scolex comprised of 4 bothridia, but rhinebothriidean bothridia are distinctive in that they are borne on stalks. With the possible exception of Pseudanthobothrium, bothridea each bear facial loculi and in many cases also an apical sucker. The larval apical organ degenerates in most species during transformation to the adult stage. The exceptions are Pseudanthobothrium and Echeneibothrium; they retain this feature in the form of the adult myzorhynchus. The order includes 111 species in 20 genera (including the 4 undescribed genera of Healy et al., 2009). Rhinebothriideans range in size from 1 mm to 3 cm in total length. A family-level classification for the order is currently lacking, but reconfiguration of membership of the Rhinebothriinae and Echeneibothriinae, may serve to accommodate at least some genera once the generic interrelationships are more fully understood. Both the analyses of Healy et al. (2009) and Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014) included

representation of 13 of the 20 genera and yielded 1 clade consisting of Anthocephalum and the 4 undescribed genera of Healy et al. (2009), and a clade consisting of the remaining genera except for Echeneibothrium. The position of the latter genus was unstable across analyses. The order is entirely restricted to, and broadly distributed across, batoids. Species have been reported from all myliobatiform families except Gymnuridae, Plesiobatidae, and Hexatrygonidae; from all rhinopristiform families except Rhinidae; and from all but the least speciose of the 3 families of Rajiformes, the Anacanthobatidae. None of the 4 families of Torpediniformes has been reported to host the order. The order is cosmopolitan in distribution, with greatest diversity in tropical and subtropical regions. However, Pseudanthobothrium and Echeneibothrium appear to have a particular affinity for cooler waters. Rhinebothriideans are common members of the faunas of freshwater stingrays throughout South America (e.g., Mayes et al., 1981; Brooks et al., 1981; Reyda, 2008; Reyda and Marques, 2011) and Borneo (Healy, 2006b). Specificity of marine species appears to be oioxenous. There is some evidence that specificy may be more relaxed in species occurring in the freshwaters of South America (e.g., Reyda, 2008; Reyda and Marques, 2011). ‘‘TETRAPHYLLIDEA’’ Carus, 1863 (Fig. 1I, J) The ‘‘tetraphyllideans’’ remain the most problematic of the cestodes associated with elasmobranchs from the standpoint of their phylogenetic relationships and thus also with respect to ordinal placement of a number of genera. All evidence indicates that the 30 genera and their 90 constituent species that were retained as ‘‘tetraphyllideans’’ by Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014), do not represent a single monophyletic group. Figure 3 illustrates the uncertainty in the phylogenetic relationships of the 21 genera they found to be interspersed among the other cestode orders, a fact that is reflected in the diversity of morphologies they exhibit. As it stands, the ‘‘Tetraphyllidea’’ comprises genera with bothridial hooks (e.g., Calliobothrium, Megalonchos, Yorkeria, Spiniloculus, Pedibothrium, Balanobothrium, and Pachybothrium), but that are not necessarily each others’ closest relatives. Also included are genera with a pair of bothridial muscular projections (e.g., Dinobothrium and Ceratobothrium) and genera (e.g., Rhoptrobothrium and Myzocephalus) bearing scolex rami (sensu Jensen and Caira, 2006). Some genera exhibit scoleces that bear a striking resemblance to those of the Phyllobothriidea (e.g., Crossobothrium and Clistobothrium), other genera (e.g., Caulobothrium, Duplicibothrium, and Dioecotaenia) have scoleces that bear a strong resemblance to those of the Rhinebothriidea; but in neither case do these genera group with the members of the order they resemble. Presumably, analyses that will include additional molecular markers and denser sampling of these and the 9 remaining genera will help to resolve these relationships. The majority of ‘‘tetraphyllidean’’ genera are associated with 5 orders of sharks: the lamniform families Lamnidae (i.e., cestode genera such as Clistobothrium and Ceratobothrium) and Cetorhinidae (i.e., Dinobothrium); the carcharhiniform families Triakidae (i.e., Calliobothrium), Carcharhinidae (i.e., Anthobothrium), and Hemigaleidae (i.e., Megalonchos); the squaliform family Squalidae (i.e., Trilocularia); the hexanchiform family Hexanchidae (i.e., Crossobothrium); a large proportion is associated with the orectolobi-


form families Brachaeluridae (i.e., Carpobothrium), Ginglymostomatidae (i.e., Pedibothrium, Pachybothrium, and Balanobothrium) and Hemiscylliidae (i.e., Yorkeria and Spiniloculus). The batoid-hosted genera parasitize only Myliobatiformes, specifically of the families Myliobatidae (i.e., Rhoptrobothrium and Myzocephalus); Rhinopteridae (i.e., Duplicibothrium and Dioecotaenia) and Dasyatidae (i.e., Caulobothrium and New genus 9). All evidence suggests that species in these genera exhibit oioxenous specificity for their hosts. Further generalizations regarding the ‘‘tetraphyllideans’’ will be more meaningful in the context of a clearer picture of their true affinities. TRYPANORHYNCHA Diesing, 1863 (Fig. 1B) The Trypanorhyncha is the most specious elasmobranch-hosted cestode order; to date, 303 species in 81 genera are recognized as valid. A considerable number of species and as many as 14 genera are known from larval stages in intermediate hosts, mainly teleosts; the elasmobranch definitive host for these remains to be determined. Overall, the most specious genera in the order are the tentaculariid Nybelinia with 28 species, and the eutetrarhynchid Dollfusiella with 26 species, whereas a number of genera (e.g., Fellicocestus, Mixodigma, and Nataliella) are monotypic. Trypanorhynchs are characterized by their possession of a scolex with 2 or 4 bothria and a complex rhyncheal apparatus including 4 armed tentacles, tentacle sheaths, and retractor muscles. The rhyncheal apparatus is a true synapomorphy for the group, although species in the genera Aporhynchus and Nakayacestus have secondarily lost this feature altogether. The smallest species are approximately 1 to 2 mm in total length (see Palm, 2004), but species longer than 30 cm are not uncommon (e.g., species of Sphyriocephalus, Nybelinia, and Fellicocestus). Most species parasitize the spiral intestine of their elasmobranch host, but some such as the Tentaculariidae reside in the stomach and a few have been reported from the gall bladder (Fellicocestus) or nephridial system (Mobulocestus) (Campbell and Beveridge, 2006). The Trypanorhyncha is the only group of elasmobranch cestodes in which strict host specificity at the species level is not the general pattern. Although some species have been reported from but a single host species, others parasitize elasmobranchs representing as many as 4 orders (see Palm, 2004; Palm and Caira, 2008). Members of all but the following 7 shark and 5 batoid families have been reported to host trypanorhynchs: Echinorhinidae, Brachaeluridae, Rhincodontidae, Mitsukurinidae, Pseudocarchariidae, Proscylliidae, and Leptochariidae; and Narkidae, Anacanthobatidae, Platyrhinidae, Zanobatidae, and Hexatrygonidae. Collectively, the Trypanorhyncha are likely the most cosmopolitan of elasmobranch-hosted cestode groups; they parasitize elasmobranchs in both the marine and freshwater environment. Even individual species have been demonstrated to have a cosmopolitan distribution (Palm et al., 2007). Several comprehensive treatments of the group have focused either on classification (Dollfus, 1942; Campbell and Beveridge, 1994; Palm, 2004) or phylogenetic interrelationships based on molecular sequence data (Palm et al., 2009; Olson et al., 2010). Historically, classification schemes have differed depending on the importance placed or tentacular armature versus other morphological features by respective authors. As it stands, 2 suborders are recognized: the Trypanobatoida and Trypanoselachoida primar-

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ily parasitizing, as their names suggest, batoids and sharks, respectively. These phylogenetic efforts demonstrated that some of the 15 families recognized by Palm (2004) (i.e., Lacistorhynchidae, Eutetrarhychnidae, Gymnorhynchidae, Gilquiniidae, and Otobothriidae) are not monophyletic and are in need of revision. Given the ubiquity of trypanorhynchs across host taxa and geographies, the species diversity of this group to date is grossly underestimated. PHYLOGENETIC RELATIONSHIPS The reconfiguration of cestode classification, from the 4 orders parasitizing elasmobranchs recognized by Khalil et al. (1994) (i.e., Trypanorhyncha, Diphyllidea, Lecanicephalidea, and Tetraphyllidea) to the 9 orders treated above, is entirely a result of the dismantling of the Tetraphyllidea. All phylogenetic analyses have shown the latter order to be paraphyletic (e.g., Euzet et al., 1981; Brooks et al., 1991; Hoberg et al., 1997; Mariaux, 1998; Caira et al., 1999, 2001, 2005; Olson and Caira, 1999; Kodedova´ et al., 2000; Olson et al., 2001; Waeschenbach et al., 2007, 2012; Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014). The formal dismantling of the Tetraphyllidea occurred in stages. Olson and Caira (2001) resurrected the Litobothriidea of Dailey (1969). Caira et al. (2005) resurrected the order Cathetocephalidea of Schmidt and Beveridge (1990). Healy et al. (2009) established the new order Rhinebothriidea. The molecular phylogenetic analysis of Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014), in large part because of the breadth of its taxon sampling (i.e., 68 of the 110 acetabulate genera parasitizing elasmobranchs) confirmed these previous actions and resulted in establishment of the additional new orders Phyllobothriidea and Onchoproteocephalidea. Unfortunately, despite all efforts to circumscribe monophyletic orders, several genera or groups of genera remain distributed among the established acetabulate orders, requiring retention of a paraphyletic ‘‘Tetraphyllidea’’ sensu stricto; the affinities of these taxa with respect to one another and to all other cestode orders are unclear because not only was support for their inclusion in any of the larger clades low, but they were also found to be labile in position across analyses by Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014). Nonetheless, resolution of some elements of the interrelationships among the monophyletic elasmobranch-hosted orders has resulted from efforts to explore cestode interrelationships overall (e.g., Olson et al., 2001; Waeschenbach et al., 2007, 2012; Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014). The more stable aspects of these are summarized in Figure 3. The bothriate orders, which include the trypanorhynchs and diphyllideans, consistently group outside of the acetabulate orders, although stability in their interrelationships has yet to be achieved. The Litobothriidea is sister to a robust clade consisting of the acetabulate orders, a relationship supported by the presence of an apical organ at some time in development. The position of the cathetocephalideans among the acetabulate taxa in the analysis of Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014) is interesting given the unusual non-acetabulate scolex morphology of members of the order. This placement differs from that presented by Caira et al. (2005), but it seems more probable given that the analyses of Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014) were based on both more data and a much

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greater sampling of taxa. Among the acetabulate orders, the Lecanicephalidea is likely basal. With respect to the other acetabulate groups, the relationships among the Phyllobothriidea, Onchoproteocephalidea, residual ‘‘Tetraphyllidea,’’ and a clade comprising the Cyclophyllidea, Tetrabothriidea, Nippotaeniidea, and Mesocestoides require further investigation. Members of the latter clade parasitize mammals and birds (and teleosts in the case of the few known nippotaeniid species); the majority of hosts are terrestrial. Yet, Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014) provided evidence that an elasmobranch-hosted genus (e.g., Carpobothrium) is the likely sister taxon to the clade, suggesting that cestode associations with terrestrial hosts (and mammals and birds in particular) are derived from elasmobranch-hosted marine ancestors. Clearly, more dense taxon sampling and additional markers are required to resolve these relationships more fully. Nonetheless, there can be no doubt that the tapeworms of elasmobranchs are foundational elements of cestode evolution. KEY MORPHOLOGICAL FEATURES Historically, the scolex of cestodes has been characterized as bearing bothria, bothridia, or suckers, with the latter 2 terms often being used synonymously with acetabula. However, the fundamental distinction among these structures has often been overlooked in the presence of other distractingly complex features of the scolex such as apical organs or the rhyncheal apparatus. As a consequence, the term bothridium has often been casually applied without consideration of structure, even within the past few decades, for example as was done by Campbell and Beveridge (1994) and Khalil (1994) in their treatments of the trypanorhynchs and diphyllideans, respectively. In 1999, Caira and colleagues undertook a comprehensive morphological analysis across cestode orders and resurrected the distinction between bothria and bothridia made previously by authors such as Fuhrmann (1931). They reiterated that although acetabula, a term they defined as encompassing both bothridia and suckers, are membrane-bounded structures consisting of radial muscle fibers extending between the tegument and the bounding membrane, bothria entirely lack this configuration. They noted that unlike the scoleces of the Lecanicephalidea and ‘‘Tetraphyllidea’’ which bear acetabula in the form of bothridia or suckers, those of the Diphyllidea and Trypanorhyncha bear bothria. The ubiquity of bothria across trypanorhynchs was later confirmed by Jones et al. (2004) and across diphyllideans by Tyler (2006). This distinction was of key importance for it brought to light a fundamental plesiomorphic morphological similarity between the Trypanorhyncha and Diphyllidea, and other bothriate orders such as the Diphyllobothriidea and Bothriocephalidea (then collectively referred to as the Pseudophyllidea). Simultaneously, it revealed the potentially synapomorphic nature of acetabula for a clade of other orders. Molecular support for this notion abounds (e.g., Olson et al., 2001; Waeschenbach et al., 2007, 2012), and the presence of acetabula is now considered a synapomorphy for the immense clade consisting of the majority of other cestode taxa, including Lecanicephalidea, Rhinebothriidea, Phyllobothriidea, Onchoproteocephalidea, Cyclophyllidea, Tetrabothriidea, and the residual tetraphyllideans (Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014). The lack of

acetabula in the Cathetocephalidea and Nippotaeniidea is considered to represent a loss in both cases. The homology of apical structures across acetabulate orders is also now apparent. This feature appears to have arisen in the common ancestor of the Litobothriidea and the acetabulate clade, and to have been lost in the Cathetocephalidea (Fig. 3). Thus, the rostellum of cyclophyllideans and some onchoproteocephalideans, the apical organ of lecanicephalideans, and the myzorhynchus of rhinebothriideans such as Echeneibothrium are homologous. In many rhinebothriideans, phyllobothriideans, and onchoproteocephalideans, this organ degenerates in the transformation to the adult form. But, its presence in the larval stages of many of these is well documented (see Jensen and Bullard, 2010). Although hooks occur across cestodes, when interpreted in a phylogenetic framework it is now apparent that they are not necessarily homologous across orders. This result allows 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 elasmobranch cestodes, armature is seen on the apex of the scolex of some diphyllideans, on the tentacles of trypanorhynchs, as well as on some of the bothridiate onchoproteocephalideans and 3 clades of ‘‘tetraphyllideans’’ (i.e., Calliobothrium species, Megalonchos species, and the clade containing Pedibothrium and its relatives). Hooks are also seen on the rostellum of many cyclophyllideans and on the bothria of a few bothriocephalideans. When armature is mapped onto the phylogenetic tree presented by Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014) (Fig. 3), it appears that hooks may have evolved independently on at least 8 occasions. The non-homology of armature across cestodes is supported by our data on the amino acid composition of hooks. Early work on cyclophyllidean hooks (e.g., Gallagher, 1964; Dvorak, 1969) showed them to be comprised of a keratin-like protein, signaled by a relatively high cystine content. The amino acid profile we generated for the hooks of a replicate cyclophyllidean species (i.e., Taenia pisiformis) was very much like that reported by Gallagher (1964) for Echinococcus granulosus (Fig. 4A) and also that reported by Dvorak (1969) for Taenia taeniaeformis. Analysis of the amino acid composition of the hooks of exemplars of 6 of the other 7 hooked cestode groups (Fig. 4B-L) points to remarkable compositional similarities within lineages but substantial differences among lineages. In all cases, the non-cyclophyllidean lineages exhibited amino acid profiles indicative of proteins other than keratin, but these proteins have yet to be identified. The hooks of trypanorhynchs are particularly intriguing for both species analyzed exhibited amino acid profiles that were remarkably high in histidine (i.e., 59–70.6% of total amino acids). It seems likely that the hook proteins exhibited by some groups (e.g. trypanorhynchs) may be novel and thus represent particularly fruitful areas for further investigation. Scanning electron microscopy across the class has confirmed microtriches as a synapomorphy for cestodes (see Chervy, 2009 and references therein). Happily, cestodologists have now reached consensus regarding a standardized terminology for the various forms of these unique tegumental extensions, distinguishing a small type, referred to as a filithrix, from a large type, referred to as a spinithrix. In total, 3 forms of filitriches and 25 forms of spinitriches are recognized. Microthrix form and terminology


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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 interesting that much of the substantial variation seen in spinitriches occurs among the tapeworms of elasmobranchs; they collectively exhibit 21 of the 25 spinithrix forms recognized. Members of the Trypanorhyncha, Diphyllidea, Lecanicephalidea, and a subset of the Phyllobothriidea are particularly spectacularly ornamented.

GENERAL HOST ASSOCIATIONS With only a few exceptions (e.g., Kennedy, 1965), adult cestodes parasitize vertebrates. Given the unresolved nature of the base of the cestode tree, determination of the vertebrate group first parasitized is not currently possible. What is clear, however, is that elasmobranchs, once parasitized, served as the source of essentially all acetabulate taxa that subsequently went on to

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parasitize freshwater or terrestrial hosts. Furthermore, it appears this may have happened on as few as only 2 occasions. Within the Onchoproteocephalidea, taxa previously referred to the order Proteocephalidea, which collectively parasitize a diversity of freshwater teleosts, a few turtles, and some members of terrestrial groups such as lizards, snakes, and an opossum (see CanedaGuzman et al., 2001), appear to represent a monophyletic group with respect to the members of the order that parasitize batoids of euryhaline or even freshwater habitats (see Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014). The second instance involves the well-supported clade containing the Tetrabothriidea, Nippotaeniidea, Mesocestoides, and the remarkably speciose Cyclophyllidea. This clade is often referred to as the ‘‘terrestrial clade’’ because the majority of its members parasitize terrestrial birds, mammals, and snakes, with only a few hosted by marine birds and mammals, and freshwater fishes. While the specific elasmobranch-hosted taxon that is sister to the ‘‘terrestrial’’ clade is unclear, all of the likely candidates given the topologies of the Caira, Jensen, Waeschenbach, Olson, and Littlewood (2014) trees (e.g., Carpobothrium, their New genus 9, Caulobothrium, Dinobothrium þ Ceratobothrium, Pedibothrium and its relatives) are parasites of elasmobranchs, and with the exception of New genus 9, are all parasites of sharks. With respect to the marine members of that clade, Hoberg (1995, 1996) has made a strong case that ‘‘terrestrial’’ presence of tetrabothriideans in marine hosts is the result of 1 or possibly more colonization events involving marine taxa. ASSOCIATIONS WITH ELASMOBRANCHS Our understanding of diversity and interrelationships within the Elasmobranchii has improved substantially over the past 20 yr. Over that time, approximately 300 elasmobranch species have been resurrected or described (White and Last, 2012), bringing the known number of species in the subclass to approximately 1,200. The first comprehensive molecular phylogeny, generated using a single gene approach, is now available (Naylor, Caira, Jensen, Rosana, Straube, and Lakner, 2012). This work is being significantly expanded upon by inclusion of additional markers and taxa with support from NSF’s AToL program (G. Naylor, pers. comm.). The Naylor, Caira, Jensen, Rosana, Straube, and Lakner (2012) tree provides support for the mutual monophyly of 2 major groups of elasmobranchs, the batoids (i.e., stingrays and their relatives) and the selachians (i.e., sharks). At present 12 orders (4 batoid and 8 shark), 54 families (20 batoid and 34 shark), and 195 genera (89 batoid and 106 shark) of elasmobranchs are recognized (Ebert et al., 2013). Within elasmobranchs, the tapeworm faunas of near-shore, shallow-water taxa are most well studied. However, tapeworms have been reported from all 12 elasmobranch orders. At least 1 species in all 20 batoid families has been examined for, and found to host, cestodes. Among sharks, at least 1 species in 28 of the 34 families has been examined for cestodes, but the faunas of the Proscylliidae, Pseudocarchariidae, Rhincodontidae, Oxynotidae, Echinorhinidae, and Chlamydoselachidae are completely unknown. All but 2 of the 28 shark families examined are known to host cestodes. The exceptions are the Leptochariidae and Pseudotriakidae. Neither group is particularly speciose; the former is monotypic and the latter includes only 4 species in 3 genera. Examination of 34 specimens of Leptocharias smithii off Senegal, 3 specimens of Pseudotriakis microdon from the Azores, and 6

specimens of Gollum attenuatus from New Zealand yielded no tapeworms. From the standpoint of species coverage, by far the most poorly known faunas are those of all 3 families of skates and the catsharks (‘‘Scyliorhinidae’’; shown to be non-monophyletic by Naylor, Caira, Jensen, Rosana, Straube, and Lakner, 2012). Although elasmobranchs are primarily marine, and as a consequence, so too are their cestodes, some have the ability to enter estuarine waters, and several groups have made independent incursions into truly freshwater environments. Notable among these is the Potamotrygonidae, all members of which are endemic to rivers of South America. Other freshwater elasmobranchs belong to genera that are entirely freshwater (e.g., Glyphis), or predominantly freshwater (e.g., Pristis), or that are otherwise entirely marine (e.g., Dasyatis and Himantura). Work on the cestodes of potamotrygonids was pioneered by Brooks and his collaborators (e.g., Brooks et al., 1981; Mayes et al., 1981) and has expanded to include all major river basins (e.g., Marques et al., 2003; Luchetti et al., 2008; Menoret and Ivanov, 2009; Reyda and Marques, 2011). Cestodes have also been reported from Pristis pristis (as P. perotteti) in Lake Nicaragua (e.g., Watson and Thorson, 1976) and from Himantura polylepis (as H. chaophraya) in the Kinabatangan River in Borneo (e.g., Fyler and Caira, 2006; Healy, 2006b). Much remains to be learned about cestodes of freshwater sharks and batoids. Many cestode genera and even some cestode orders are restricted to elasmobranch orders, families, or in some cases genera. The challenge is to determine which level applies to which cestode group. These associations are most well illustrated at the level of cestode genus because generic monophyly has been the focus of a substantial amount of recent revisionary systematic work. The following examples illustrate this point. With respect to host genus fidelity, the lecanicephalidean Eniochobothrium parasitizes only cownose rays of the genus Rhinoptera (see Jensen, 2005) and the ‘‘tetraphyllidean’’ Yorkeria parasitizes only bamboo sharks of the genus Chiloscyllium (see Caira et al., 2007). With respect to host family fidelity, the lecanicephalidean Tetragonocephalum parasitizes only stingrays of the family Dasyatidae (see Jensen, 2005) and the onchoproteocephalidean Platybothrium parasitizes only sharks of the family Carcharhinidae (see Healy, 2003). The cathetocephalidean Cathetocephalus is also restricted to this host family (Caira et al., 2005). Litobothrium parasitizes only 3 of the 7 families of lamniform sharks; as it is the only genus in its order, the order Litobothriidea is thus also restricted to these families (Olson and Caira, 2001). The significance of understanding these affiliations is that once the nature and level of host associations have been determined, robust predictions about the cestode faunas of host taxa not yet examined can be made. At the species level, specificity is usually much tighter. For the most part, cestodes of elasmobranchs exhibit oioxenous (i.e., species-specific) associations with their hosts. This has been observed in onchoproteocephalideans (e.g., Caira and Jensen, 2001, 2009; Fyler et al., 2009), diphyllideans (Tyler, 2006; Caira, Marques et al., 2013), litobothriideans (Olson and Caira, 2001), cathetocephalideans (Caira et al., 2005), rhinebothriideans (Healy, 2006a), lecanicephalideans (Jensen, 2005), phyllobothriideans (Ruhnke, 2011), and ‘‘tetraphyllideans’’ (e.g., Caira et al., 2004, 2007); in many of these instances confirmation has been provided using molecular data. The situation in trypanorhynchs diverges from this pattern. The assessment of host specificity by Palm and Caira (2008) using the Host Specificity


index (HSs) of Caira et al. (2003) yielded a mean index value of 3.86 for the 63 species of adult trypanorhynchs examined, as compared to a value of 0 for the oioxenous taxa typical of the other orders (Caira et al., 2003). As specific examples, Grillotia erinaceus has been reported from several orders of batoids and sharks, as has Lacistorhynchus dollfusi (see Palm, 2004). Thus, for a reason that is not yet understood, host specificity in the Trypanorhyncha appears to be more relaxed than it is in any of the other elasmobranch-hosted orders. As a consequence, trypanorhynch specificity at categories of classification above species also appears to be more relaxed and thus also less predictable. LIFE CYCLES The life cycles of elasmobranch tapeworms are particularly poorly known, a fact that is reiterated each time the subject has been raised (e.g., Chambers et al., 2000; Chervy, 2002; Palm, 2004; Caira and Reyda, 2005; Jensen, 2005; Jensen and Bullard, 2010). A complete life cycle has yet to be established for even a single species in nature, although Sakanari and Moser (1989) completed the life cycle of the trypanorhynch Lacistorhynchus dollfusi experimentally. It is generally thought that elasmobranch cestodes parasitize 2 or perhaps 3 different intermediate host species before their elasmobranch definitive host. The existence of a fourth intermediate, or possibly paratenic, host has been suggested in some cases (e.g., Palm, 2004). Life cycle stages are trophically transmitted between hosts in the life cycle sequence. Taxa serving as intermediate or possibly paratenic hosts in the marine environment were summarized by Caira and Reyda (2005). Life cycle work is severely hampered by the difficulties associated with identifying cestode larvae to species, or in some cases even to higher taxon level. The notable exception is the Trypanorhyncha. The presence of a fully armed rhyncheal apparatus, which is diagnostic at the species level, allows for identification of trypanorhynch larvae to species in intermediate hosts, be they teleosts, molluscs, crustaceans, jellyfishes, or sea cucumbers (see Palm, 2004). In contrast, the literature is rife with reports of cestode larvae that lack the rhyncheal apparatus and thus are of unknown or uncertain identity, from a wide array of marine animals (see Dollfus, 1976; Chambers et al., 2000; Caira and Reyda, 2005; Jensen and Bullard, 2010, and references therein). Recent applications of molecular methods have substantially improved the situation, for they have allowed morphologically amorphous or divergent larval forms to be associated with their adult counterparts. Much of this work has focused on specific larval types found in squid (e.g., Brickle et al., 2001; Randhawa and Brickle, 2011), cetaceans (e.g., Agusti et al., 2005; Aznar et al., 2007; Randhawa, 2011), the cephalochordate Amphioxus (Holland et al., 2009), and bivalves (e.g., Holland and Wilson, 2009). A more comprehensive approach was taken by Jensen and Bullard (2010) who generated partial (i.e., D1-D3) 28S ribosomal DNA sequence data for 25 species of adult cestodes from elasmobranchs and 27 larval cestode species from teleosts, molluscs, and shrimps in the Gulf of Mexico. Their work led to the identification of specific larval forms that could be confidently assigned to rhinebothriidean, ‘‘tetraphyllidean,’’ and also what are now recognized as phyllobothriidean and onchoproteocephalidean genera. Among other inroads, their work revealed the

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much larger role teleosts play in the life cycles of many of these taxa than suspected. The key to larval types provided by Jensen and Bullard (2010), which was generated using both morphological and molecular data, provides guidance for future such work. Longevity of tapeworms in elasmobranchs has yet to be assessed with certainty. Existing indirect evidence suggests they are much shorter lived than cestodes that parasitize mammals, which are considered to live for up to decades (e.g., Read, 1967; Roberts et al., 2013). Evidence comes from seasonal studies involving large sample sizes, such as those of McCullough et al. (1986) and Pickering and Caira (2014), in which prevalence and intensity of infections of cestodes parasitizing Squalus acanthias declined sharply at certain times of the year, which is consistent with the death of worms on an annual basis. Work examining cestode faunal compositions in individuals of the stingray Dasyatis americana of different ages (T. Mattis, pers. comm., in Caira, 1990), showing that faunas turn over, rather than expand over time, supports individual worm longevity of several years at most. GEOGRAPHICAL DISTRIBUTION Given that tapeworms are ubiquitous residents of the spiral intestine of elasmobranchs and elasmobranchs are found around the globe, it is not unexpected that their tapeworms are also global in distribution. Elasmobranch cestodes from the coastal waters off Europe (e.g., Rudolphi, 1819; van Beneden, 1850; Dollfus, 1942; Williams, 1959) and North America (e.g., Linton, 1889, 1890, 1908, 1924) were among the first documented. Cestodes are now known from elasmobranchs in all major ocean basins and Antarctic (e.g., Wojciechowska, 1990) and arctic (J. Caira, pers. obs.) waters. They have been reported from the Mediterranean Sea (e.g., Euzet, 1959), Black Sea (Vasileva et al., 2002), Baltic Sea (Rudolphi, 1819), North Sea (e.g., McVicar, 1976), Red Sea (e.g., Ramadan, 1984), Persian Gulf (e.g., Malek et al., 2010), Gulf of Mexico (e.g., Jensen, 2009), and Gulf of Thailand (e.g., Caira and Tracy, 2002). There are records from waters surrounding oceanic islands such as Taiwan (e.g., Fyler, 2011), New Caledonia (e.g., Beveridge and Justine, 2010), Kiribati (Richmond and Caira, 1991), Galapagos Islands (Nock and Caira, 1988), Solomon Islands (Cielocha et al., 2013), the Azores (e.g., Noever et al., 2010; Caira and Pickering, 2013), Japan (e.g., Yamaguti, 1934, 1952), as well as larger islands such as Iceland (e.g., Beveridge and Campbell, 2007), Greenland (Baer, 1956), and New Zealand (e.g., Robinson, 1959). Some of the most well characterized elasmobranch cestode faunas are now those of Australia (e.g., Campbell and Beveridge, 2002; Beveridge and Campbell, 2005; Ruhnke, Healy, and Shapero, 2006; Caira et al., 2007; Cielocha and Jensen, 2013), the Gulf of California (e.g., Jensen, 2001; Tyler, 2001; Ghoshroy and Caira, 2001; Campbell and Beveridge, 2006), and Borneo (e.g., Ruhnke, Caira, and Carpenter, 2006; Koch et al., 2011; Schaeffner et al., 2011). With respect to South America, records exist from both the western coast (e.g., Carvajal and Dailey, 1975; Campbell and Carvajal, 1987) and eastern coast (e.g., Ivanov and Campbell, 2002; Ivanov and Brooks, 2002). In addition, as noted above, cestodes are known from elasmobranchs in all of the major river basins of South America, several rivers of Borneo, and Lake Nicaragua.

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With the exception of a few records from South Africa (e.g., Palm, 1999; Caira, Rodriguez, and Pickering, 2013), Madagascar (e.g., Caira and Rasolofonirina, 1998; Jensen and Caira, 2008), and Senegal (e.g., Caira, Rodriguez, and Pickering, 2013; Jensen et al., In Press), data on elasmobranch cestodes from the coasts of many African countries are extremely limited. But, by far the most problematic regions of the world are the coastal waters surrounding India and Sri Lanka. The reasons for this are twofold. First, some of the earliest comprehensive work on elasmobranch cestodes was conducted off Sri Lanka (then Ceylon) (e.g., Shipley and Hornell, 1905, 1906; Southwell, 1911, 1912, 1925, 1929, 1930a, 1930b) in conjunction with the Britishfunded pearl oyster industry. Although the majority of the descriptions in these works are reasonably detailed and well illustrated, it is often difficult to place them into modern taxonomic schemes, and unfortunately, much of the type material associated with these works is missing. Shipley and Hornell’s material is lost and although some of Southwell’s specimens are deposited at the Natural History Museum in London, that is not the case for most of his material. However, the work of Subhapradha (e.g., 1955) aside, of even greater concern is the substantial number of problematic, very superficial and poorly illustrated descriptions of elasmobranch tapeworms that have come from India in the last approximately 40 yr. Of the more than 150 species described from that region since 1979, almost 30% have already been determined to be species inquirenda, nomina nuda, or synonyms; the remainder has yet to be verified. Host identifications for most species are questionable, even at the genus level. What is even more problematic is the complete lack of type material of these species available for study. Recollection of essentially all species will be needed to rectify this situation. CESTODE ASSEMBLAGES Cestodes comprise by far the majority of the fauna parasitizing the spiral intestine of most elasmobranch taxa (e.g., Cislo and Caira, 1993; Curran and Caira, 1995), with nematodes, in addition to the occasional digenean, acanthocephalan, and rarely monogenean occurring in some (Caira et al., 2012). Examination of the spiral intestine of any elasmobranch anywhere in the world is likely to yield cestodes, for they are essentially ubiquitous. Cestode infections can range from a single to thousands of individuals in a single host specimen. Cestode faunal complexity varies widely across elasmobranch groups. By far the most complex and diverse cestode assemblages are seen in batoids, and in particular in species of Dasyatidae (stingrays) and Myliobatidae (eagle rays). The cooccurrence of multiple congeners, several genera in the same order, and representatives of several orders is common in even a single host individual. For example, the eagle ray Aetobatus ocellatus may host as many as 28 species of cestodes (White et al., 2010; Mojica et al., 2014) representing what are now recognized as 5 orders and 19 genera of tapeworms. Admittedly, in the past, issues with misidentification of congeneric hosts involving morphologically similar or even cryptic species have plagued assessments of host specificity and concomitantly determinations of cestode assemblage diversity (e.g., Fyler and Caira, 2010). As efforts to resolve and stabilize elasmobranch taxonomy continue (White and Last, 2012), the issue of host identification is becoming more tractable, particularly if the protocol for host tracking outlined below becomes more widely adopted.

By far the most depauperate faunas are those of deeper water sharks (e.g., Caira and Pickering, 2013). At this point it is not entirely clear whether there is a phylogenetic component to this phenomenon, for the majority of deeper water sharks belong either to the order Squaliformes (dogfish sharks) or the carcharhiniform family ‘‘Scyliorhinidae’’ (catsharks). Nonetheless, both prevalence and intensity of infection is extremely low, and these elasmobranchs typically harbor infections that consist of only a single species of tapeworm. TRACKING ELASMOBRANCH HOSTS AND IDENTITIES The fact that more than 300 elasmobranch species have been described or resurrected over the past 20 yr underscores the importance of verifying the identities of elasmobranch specimens from which tapeworms are collected. As many of the more taxonomically problematic elasmobranchs belong to common genera that were among the first reported to host tapeworms, they challenge many historical host records. Such genera include, for example, Squalus (see Last et al., 2007), Aetobatus (see White et al., 2010), and Pastinachus (see Last and Manjaji-Matsumoto, 2010). In many cases, confirmation of host associations requires collection of new cestode material from hosts of verified identity. Moving forward, a standard method for documenting elasmobranch host identities must be used. In collaboration with elasmobranch biologists, we have developed a DNA-based approach for verifying elasmobranch species identities that has involved generation of sequence data for approximately 1,000 base pairs of the mitochondrial protein-coding gene NADH dehydrogenase subunit 2 (NADH2; see Naylor, Caira, Jensen, Rosana, Straube, and Lakner, 2012; Naylor, Caira, Jensen, Rosana, White, and Last, 2012; Straub et al., 2013) for multiple individuals representing more than 575 verified elasmobranch species across the Elasmobranchii, many of which were sampled for cestodes. Reference sequence data for this gene for these species are now available in GenBank (see Naylor, Caira, Jensen, Rosana, Straube, and Lakner, 2012; Naylor, Caira, Jensen, Rosana, White, and Last, 2012). A small sample of liver or muscle tissue is now routinely collected from all host specimens examined and NADH2 data are generated and compared to this library for confirmation of specific identity. Work towards generating and depositing NADH2 sequence data for all elasmobranch species continues. As a consequence, the GenBank library continues to expand. To corroborate molecular-based identifications, we have established a publicly available on-line database for housing images and data for each host specimen examined (elasmobranchs.tapewormdb.uconn.edu). In the field, each host specimen is assigned a unique combination of Collection Code and Collection Number (e.g., BO-11) and a series of digital photographs is taken along with basic morphometric data. Once uploaded to the database, this unique record allows each host specimen and its associated cestodes (and other parasites) to be easily tracked, while facilitating comparisons of data and images across host specimens. Although labor-intensive, we urge future workers to consider following this protocol for all elasmobranch specimens serving as hosts, for the benefits in terms of accuracy and longevity/stability of host identifications cannot be overemphasized. We note that others have generated cytochrome c oxidase subunit I (COI) data to employ a DNA-barcoding approach to recognize species boundaries in elasmobranchs (e.g.,


Ward et al., 2008); however, the reference library for NADH2 is more extensive and includes more vouchered (either with photographs or museum specimens) elasmobranch species. OTHER CONSIDERATIONS Although studies documenting and describing parasite and host diversity and phylogenetic relationships dominate the elasmobranch-tapeworm literature, other aspects of this system have been explored. These other areas are highlighted below, focusing on more recent work. However, we would be remiss in this review if we did not mention the wonderfully detailed works of Rees and Williams (e.g., Rees, 1941, 1946, 1959, 1961; Rees and Williams, 1965; Williams, 1966) that have contributed substantially to our understanding of the functional morphology of a variety of elasmobranch cestodes. Ultrastructural investigations of elasmobranch tapeworms using transmission electron microscopy have elucidated details of scolex and strobilar morphology and anatomy. The central nervous system has been characterized in trypanorhynchs (Biserova, 2008; Biserova and Korneva, 2012). Ultrastructural elements of spermiogenesis and/or spermatozoa are among the most well studied features; this body of work was reviewed by Levron et al. (2010). Most recently, work has focused on diphyllideans (Marigo et al., 2011a), lecanicephalideans (Cielocha et al., 2013), onchoproteocephalideans (Marigo et al., 2011b), but mainly trypanorhynchs (Miquel and S´widerski, 2006; Miquel et al., 2007; Marigo, S´widerski et al., 2011). Similarly, ultrastructural detail of vitellogenesis has been studied in diphyllideans (S´widerksi et al., 2011) and some trypanorhynchs (S´widerski et al., 2006a, 2006b, 2012). Regions of the scolex of diphyllideans (Biserova, 1992), ‘‘tetraphyllideans’’ (McCullough and Fairweather, 1989), and trypanorhynchs (Jones and Beveridge, 1998) have also been characterized, as has the terminal genitalia of a phyllobothriidean (Beveridge and Smith, 1985). Although cestodes are not known to cause substantial damage to their hosts, several studies have documented the pathological responses at the site of attachment to the mucosal of the spiral intestine. Cestodes involved have included trypanorhynchs (e.g., Borucinska and Caira, 1993, 2006; Borucinska and Dunham, 2000), ‘‘tetraphyllideans’’ (Borucinska and Caira, 1993), and lecanicephalideans (Borucinska et al., 2013). In addition, larval trypanorhynchs have been associated with histopathological changes at the site of their attachment to the liver of sharks (Campbell and Callahan, 1998; Cousin et al., 2003) and with lesions in the gastric wall of a cownose ray (Borucinska and Bullard, 2011). A relatively large body of work exists characterizing the mode of attachment of cestodes to the intestinal mucosa. This work has included exemplars of all 9 orders: cathetocephalideans (e.g., Caira et al., 2005), diphyllideans (e.g., Twohig et al., 2008), trypanorhynchs (e.g., Borucinska and Caira, 1993, 2006), lecanicephalideans (e.g., Jensen et al., 2011; Borucinska et al., 2013; Jensen and Russell, 2014), litobothriideans (e.g., Dailey, 1969; Caira, Jensen, Waeschenbach, and Littlewood, 2014), onchoproteocephalideans (e.g., McVicar, 1972; Williams, 1968a), phyllobothriideans (e.g., Williams, 1968b; McKenzie and Caira, 1998), rhinebothriideans (e.g., Williams et al., 1970), and ‘‘tetraphyllideans’’ (e.g., Williams et al., 2004). In general, a distinction can be made between species that either grasp or

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intercalate their scolex into existing elements of the mucosa (e.g., McKenzie and Caira, 1998) and those that physically transform the mucosa into a configuration that allows them to attach more effectively (e.g., Borucinska and Caira, 1993; Caira, Jensen, Waeschenbach, and Littlewood, 2014). Furthermore, site of attachment within the spiral intestine has been characterized either for entire cestode faunas (e.g., Cislo and Caira, 1993; Curran and Caira, 1995), or subsets of species comprising faunas (e.g., Williams et al., 1970; McVicar, 1979; Randhawa and Burt, 2008; Twohig et al., 2008). This work was often conducted in concert with investigations of mode of attachment. Studies examining the physiological basis of this host-parasite system do not date beyond those of early workers such as Read (1957), Simmons et al. (1960), and Pappas and Read (1972). This is unfortunate for we believe much is to be gained from applying more modern methods to characterize the physiology of the spiral intestine and the absorption of nutrients across the cestode tegument, especially as these might relate to attachment site specificity. Given the complexity of cestode faunas in elasmobranchs and the relative difficulty in obtaining samples and thus appropriate sample sizes, ecological aspects of this host-parasite system have been given relatively little consideration compared to freshwater and terrestrial host-parasite systems. Much of the ecological work has focused on characterization of communities and potential competition, specifically whether the assemblages interact (e.g., Kennedy and Williams, 1989; Cislo and Caira, 1993; Curran and Caira, 1995; Friggens and Brown, 2005; Alarcos et al., 2006; Keeney and Poulin, 2007; Randhawa, 2012). Elasmobranch parasite assemblages have also been used to identify diversity hotspots (Poulin et al., 2011). Seasonality of infection has been explored (McCullough et al., 1986; Pickering and Caira, 2014), as has the relationship between host and cestode body size (Randhawa and Poulin, 2009, 2010a), and species richness in relation to environmental factors and host phylogeny (Randhawa and Poulin, 2010b). The potential of elasmobranch parasites for use as biological tags was reviewed by Caira (1990); Moore (2001) and Yamaguchi et al. (2003) conducted detailed field studies exploring this potential in sharks off Great Britain and Japan, respectively. Surprisingly little work has been done exploring the coevolutionary relationships between cestodes and their elasmobranch hosts. This is in large part because robust phylogenies for elasmobranchs and their cestodes have been lacking. To our knowledge, the only published study comparing phylogenetic trees generated independently for both taxa was that of Caira and Jensen (2001) who used trees for hosts and parasite counterparts that were extremely preliminary. The pattern seen revealed a substantially greater amount of discordance than expected given the high degree of host specificity of the cestode taxa included. Documentation of the degree of coevolution in most of the elasmobranch cestode groups and ultimately the processes underlying these patterns remains 1 of the most exciting and potentially productive areas of investigation in this system. As robust and extensive species-level phylogenies for elasmobranchs (e.g., Naylor, Caira, Jensen, Rosana, Straube, and Lakner, 2012) and cestodes (e.g., Fyler, 2009; Healy et al., 2009; Palm et al., 2009; Olson et al., 2010; Caira, Jensen, Waeschenbach, Olson, and Littlewood, 2014) become more

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available, we anticipate that interest in these questions will blossom. Tapeworms and their elasmobranch hosts now constitute 1 of the most well-documented host-parasite systems known. As a consequence, this system is now poised to serve as the focus of intensive studies aimed at understanding the fundamental principles of parasite ecology, evolution, and host associations. It is our hope that the synthesis provided here will serve to pave the way for future such studies. ACKNOWLEDGMENTS We thank Al Shostak for providing hooks of Triaenophorus crassus, Gaines Tyler for hooks of Echinobothrium bonasum, and George Korza of the University of Connecticut Health Center for running the amino acid composition analyses. Elizabeth Barbeau, Lauren Abbott, and Maria Pickering provided many helpful comments on an early version of this manuscript. This work was supported in part by the National Science Foundation Planetary Biodiversity Inventory Program grants 0818696 and 0818823. Any opinions, findings and conclusions or recommendations expressed here are those of the authors and do not necessarily reflect the views of the National Science Foundation.

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Digest.

Natural infection and treatment of a dog with Mesocestoides tapeworms.

Routine establishment of primary elasmobranch cell cultures.

Prevalence and treatment of tapeworms in horses.

About people, pig movements and pork 'tapeworms'.

Pre-natal infections with larval tapeworms.

A fast exact sequential algorithm for the partial digest problem.

Isolated horizontal cells of elasmobranch retinae.

Tapeworms of the Chaco Boreal, Paraguay, with two new species.

The habenular nuclei of the elasmobranch "Scyllium stellare": myelinated perikarya.

Absence of TDP-43 is difficult to digest.

Urogynecology digest Presented by Aparna Hegde.

Urogynecology digest : presented by J. Oliver Daly.

Checklist of tapeworms (Platyhelminthes, Cestoda) of vertebrates in Finland.

March, 2013).

Characterization of a plasmin-digest fragment of rabbit immunoglobulin gamma that binds antigen and complement.

Elasmobranch pericardial function. 1. Pericardial pressures are not always negative.

Taenia solium tapeworms synthesize corticosteroids and sex steroids in vitro.

Molecular phylogeny of anoplocephalid tapeworms (Cestoda: Anoplocephalidae) infecting humans and non-human primates.

Bacterial enzymes effectively digest Alzheimer's β-amyloid peptide.

Digested disorder: Quarterly intrinsic disorder digest (July-August-September, 2013).

Urogynecology digest : presented by Omar F. Dueñas-Garcia.

The inability of macrophages to digest liposomes containing a high proportion of cholesterol.

Abdominal wall reconstruction by a regionally distinct biocomposite of extracellular matrix digest and a biodegradable elastomer.