Introduction
Cestodes make up the bulk of the intestinal helminths infecting sharks (Caira & Healy, Reference Caira, Healy, Carrier, Musick and Heithaus2012; Caira & Jensen, Reference Caira and Jensen2017) and represent, for several reasons, an ideal system to investigate the role of ecological and evolutionary factors in providing structure to parasite communities (Randhawa & Poulin, Reference Randhawa and Poulin2010; Rasmussen & Randhawa, Reference Rasmussen and Randhawa2018). First, there is substantial diversity within this parasite assemblage; over 650 spp. of tapeworms from approximately 180 genera and eight orders have hitherto been reported in sharks, and the estimated diversity is close to 1500 spp. (Caira & Jensen, Reference Caira and Jensen2017). Second, most of these species (with the exception of those belonging to the Trypanorhyncha) exhibit a high degree of host specificity, infecting a single species or a few closely-related host species (Caira & Jensen, Reference Caira and Jensen2014). Third, since cestodes are trophically-transmitted, the contacts of infective stages with sharks must be driven by both the relative degree of exploitation of the food web by these parasites (i.e. the number of intermediate and paratenic hosts they use) and by the dietary breadth of their final shark hosts (Palm & Caira, Reference Palm and Caira2008; Rasmussen & Randhawa, Reference Rasmussen and Randhawa2018). In summary, both evolutionary (e.g. specificity) and ecological (e.g. passive contacts through hosts’ diet) elements could play a variable role in defining the composition and diversity of tapeworm assemblages of sharks depending on the scale of analysis.
Over the last two decades, there has been an effort to unveil such community patterns at a global (i.e. macroecological) scale. Focusing on the component community level (i.e. samples of shark species as a whole), Randhawa & Poulin (Reference Randhawa and Poulin2010) found few consistent host effects, although tapeworm species richness was significantly influenced by shark size after correcting for host phylogenetic effects. In a recent, more detailed re-analysis, a robust pattern did emerge, that is, the diet breadth of each shark species was a strong predictor of its tapeworm species richness, with a secondary influence of other host features such as size, trophic level, taxonomic distinctness of diet, or latitudinal or depth range (Rasmussen & Randhawa, Reference Rasmussen and Randhawa2018).
In contrast, analyses at host individual (i.e. infracommunity) level are still very scarce, mainly because few parasitological surveys of sharks report on proper infracommunity parameters (e.g. mean species richness, diversity indices, or mean abundance of each tapeworm species per host). Based on a limited dataset available, Penadés-Suay et al. (Reference Penadés-Suay, Tomás, Merchán and Aznar2017) recently investigated to what extent the potential dilution’ effects of infective stages of tapeworms in the pelagic–oceanic habitat could result in comparatively species-poor, low-abundance infracommunities in large oceanic sharks, regardless of the richness in the component community locally available. These authors failed to detect this specific host habitat effect, but their literature search incidentally revealed a striking finding, that is, there were just four species of sharks (for a global diversity of approximately 500 spp.) for which quantitative surveys of the whole tapeworm fauna had been carried out in at least two localities. This is unfortunate because the comparison of local parasitological surveys at a wide geographical range, with correspondingly varied environmental conditions, could shed much light on the ecological and evolutionary determinants of richness and composition at both component community and infracommunity levels.
The blue shark, Prionace glauca (Linnaeus, 1758), is likely the shark species for which more quantitative data exist on its tapeworm fauna at a global scale. Complete surveys on cestodes have been carried out in the Mediterranean Sea (Euzet, Reference Euzet1959), the North Atlantic (Curran & Caira, Reference Curran and Caira1995; Henderson et al., Reference Henderson, Flannery and Dunne2002), and the North (Méndez & Galván-Magaña, Reference Méndez and Galván-Magaña2016; Preti et al., Reference Preti, MacKenzie, Spivey, Noble, Jones, Appy and Pierce2020) and South (Escalante, Reference Escalante1986) Pacific. In addition, a great deal of parasitological records is available from the whole distribution range of this species (online supplementary appendix S1). Some of these studies have provided interesting insights on the microhabitat distribution of tapeworms within the intestine (Curran & Caira, Reference Curran and Caira1995), tapeworm species associations (Henderson et al., Reference Henderson, Flannery and Dunne2002), or the role of host specificity in imparting similarity to faunal composition among localities (Méndez & Galván-Magaña, Reference Méndez and Galván-Magaña2016). What is lacking, however, is a comprehensive comparative analysis that accounts for the similarities and differences in composition and diversity of the tapeworm fauna, especially at infracommunity level, across localities.
In this regard, the blue shark is also an interesting species for two reasons. First, it is a highly migratory, oceanic species which is widespread in temperate and tropical waters worldwide (Compagno, Reference Compagno2001). Individual blue sharks typically perform large-scale movements, covering thousands of kilometres within a few months or even weeks (Vandeperre et al., Reference Vandeperre, Aires-da-Silva, Fontes, Santos, Serrão Santos and Afonso2014; Kai & Fujinami, Reference Kai and Fujinami2020), although substantial inter-individual variability in linear distances covered may occur (see, e.g. Stevens et al., Reference Stevens, Bradford and West2010). Second, blue sharks are generalist predators whose diet may include, not only a number of teleost and cephalopod species, but also occasionally cetaceans, birds and crustaceans (Kohler, Reference Kohler1987; Henderson et al., Reference Henderson, Flannery and Dunne2001; Biton-Porsmoguer et al., Reference Biton-Porsmoguer, Banaru, Boudouresque, Dekeyser, Béarez and Miguez-Lozano2017; and references therein). The specific diet composition has been observed to change substantially among localities, likely reflecting the relative availability of prey (Markaida & Sosa-Nishizaki, Reference Markaida and Sosa-Nishizaki2010). Thus, the tapeworm communities of blue sharks would theoretically be driven by factors tending to promote geographical similarity (i.e. a high host vagility; a narrow specificity typical from cestodes of sharks) or differentiation (a circumglobal host's geographical distribution; local variation of prey composition affecting host–parasite contacts).
Blue sharks are regularly caught by Spanish long-line fisheries operating in waters off Galicia, north-eastern Atlantic Ocean, and Valencia, eestern Mediterranean (Mejuto et al., Reference Mejuto, García-Cortés, Ramos-Cartelle and De la Serna2009a, Reference Mejuto, García-Cortés, Ramos-Cartelle and De la Sernab). This scenario provided us with the opportunity, firstly, to report on the intestinal helminth fauna of blue sharks in two new geographical areas, and to make a quantitative comparison of infracommunity data between them. Secondly, we used these data, along with those obtained for previous parasitological surveys on blue sharks worldwide, to perform a global assessment of the relative role of the ecological and evolutionary factors in structuring the local tapeworm assemblages of blue sharks.
Material and methods
Sample collection
Sampling of blue sharks was opportunistic and included both animals stranded and captured by long-line fisheries (table 1). The examination and collection of the intestines of the sharks captured by fisheries had to be carried out quickly, before the fish auction began, thus body length measurements of several individual fish could not always be taken (table 1). The intestine of 16 individuals were obtained at the port of Vigo (Galicia, Spain); this sample, which we will hereafter refer to as Galicia’, was caught by long-line fisheries operating in the north-eastern Atlantic Ocean, between 40°N 20°W and 35°N 10°W; 13 sharks were caught in October 2012, and three in May 2013. Another sample of 13 sharks was caught in the western Mediterranean, in waters off the coast of Valencia (coordinates: 39°38′N 0°44′E); this sample will be identified as Valencia (C). Finally, eight sharks were found stranded along the coast of Valencia and collected by the Valencian Community Stranding Network during the period 2013–2021; this sample will be named as Valencia (S). Blue sharks were considered juvenile when measuring less than 180 cm (males) and 220 cm (females), and adults otherwise (Compagno, Reference Compagno1984).
Table 1. Sampling features of blue sharks, Prionace glauca, collected in Iberian waters.
Note that only the range of total length (cm) was available for the sample of sharks captured in the western Mediterranean.
Due to logistic constraints, the intestine of all sharks had to be stored at −20°C for later analysis in the laboratory. After thawing, each intestine was rinsed with tap water under a 0.02 mm mesh and solid contents were collected. The intestine wall was also thoroughly examined for attached helminths. Parasites were collected under a stereomicroscope, washed in 0.9% saline, examined to describe their main features, counted, and fixed and preserved in 70% ethanol. Cestodes were stained with iron acetocarmine (Georgiev, Reference Georgiev1986), and mounted for examination. Specimens were identified based on Khalil et al. (Reference Khalil, Jones and Bray1994) and specific Refs. (Healy, Reference Healy2003; Palm, Reference Palm2004; Ruhnke & Caira, Reference Ruhnke and Caira2009; Ruhnke, Reference Ruhnke2011). Voucher specimens are deposited at the Natural History Museum of London with accession numbers: Anthobothrium caseyi, NHMUK 2022.8.31.1; Tetraphyllidea fam. gen. sp., NHMUK 2022.8.31.2; Platybothrium auriculatum, NHMUK 2022.8.31.3; Prosobothrium armigerum, NHMUK 2022.8.31.4; and Molicola horridus, NHMUK 2022.8.31.5. Additional material from these specimens and the only specimens of Scyphophyllidium sp. and Trypanorhyncha fam. gen. sp. can be found at the Collection of the Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Spain.
Statistical analyses
For each helminth taxon, we recorded its prevalence (percentage of infected hosts in the sample), mean intensity (average number of worms in the sample of hosts infected with this taxon), and mean abundance (average number of worms in the total sample of hosts) following Bush et al. (Reference Bush, Lafferty, Lotz and Shostak1997). Species richness (i.e. the number of helminth taxa per individual shark) and Brillouin's diversity index were considered as infracommunity descriptors. The 95% confidence interval (CI) for prevalence was calculated with Sterne's exact method (Reiczigel, Reference Reiczigel2003). The 95% CI for mean abundance and mean intensity of each helminth taxon, as well as for mean species richness and mean Brillouin's diversity index, were obtained with the bias-corrected and accelerated bootstrap method using 10,000 replications (Rózsa et al., Reference Rózsa, Reiczigel and Majoros2000). Kruskal–Wallis tests were used to see differences between shark samples in the abundance of 5 cestode taxa (A. caseyi, Scyphophyllidium sp., P. auriculatum, P. armigerum, M. horridus) and two infracommunity descriptors (species richness and Brillouin's diversity index).
To globally compare the infracommunity diversity and composition of cestode faunas infecting blue sharks around the world, we searched all parasitological surveys for which at least the prevalence of all tapeworm taxa found in the intestine was reported. These surveys generally did not provide data on mean species richness per host; thus we calculated this parameter by summing up prevalence (expressed as decimals) of all intestinal tapeworm taxa in each sample (Penadés-Suay et al., Reference Penadés-Suay, Tomás, Merchán and Aznar2017). Differences of prevalence of specific taxa among localities were tested with exact Chi-square tests.
We searched bibliography in the Shark References database (https://shark-references.com/species/host-parasites-list) and the Host–Parasite Database of the Natural History Museum (https://www.nhm.ac.uk/research-curation/scientific-resources/taxonomy-systematics/host-parasites/database/index.jsp) to compile all existing records of adult cestodes infecting blue sharks. The references of each publication found were also checked for potentially missed records. We selected records in which tapeworms were identified to species level and in the intestine (not the stomach or the liver), excluding taxa that had been identified only to genus level or above because they were little informative to explore specificity patterns; moreover, these taxa typically involved sexually immature forms for which blue sharks likely act as putative non-hosts. Taxonomic nomenclature was updated when necessary, using appropriate literature. For all compiled species, and also for their valid congeneric counterparts, we listed all hosts reported in the literature. The resulting inventory of host–parasite associations was placed on a cladogram of the elasmobranchs (adapted from Iglésias et al., Reference Iglésias, Lecointre and Sellos2005; Naylor et al., Reference Naylor, Caira, Jensen, Rosana, Straube and Lakner2012; Amaral et al., Reference Amaral, Pereira, Silva, Amorim and de Carvalho2018) and visually interpreted for specificity patterns.
The software PERMANOVA + for PRIMER (Anderson et al., Reference Anderson, Gorley and Clarke2008) was used to calculate infracommunity parameters, the free software ‘Quantitative Parasitology’ (Reiczigel et al., Reference Reiczigel, Marozzi, Fábián and Rózsa2019) to set the 95% CIs of infection parameters and the statistical package SPSS v. 22 for the remaining analyses (SPSS Inc., Chicago, IL). Statistical significance was set at P < 0.05.
Results
A total of 2726 helminth specimens were collected in the intestine of the 37 blue sharks, belonging to nine cestode taxa (table 2). All but one 278 cm-long male shark from Galicia harboured at least one cestode species. Adult specimens were detected in the sample of A. caseyi, P. auriculatum, P. armigerum and M. horridus, but not in the case of Tetraphyllidea spp. and Phyllobothriinae sp. 1 and 2. Only the scolex could be collected for single individuals of Scyphophyllidium sp. and Trypanorhyncha sp. and, therefore, it was not possible to confirm whether they were sexually mature. However, the length of the scolex (570 μm) and bothridia (ca. 530 μm) of Scyphophyllidium sp. was within that provided for the species specific to blue sharks, that is, Scyphophyllidium prionacis (see Ruhnke, Reference Ruhnke1994). Although we refrained to name it as such, we included it comparisons of abundance and infracommunity parameters between samples.
Table 2. Prevalence (P) expressed as percentage, and mean intensity (MI) of the cestode taxa found in the intestine of blue sharks, Prionace glauca, collected in Iberian waters.
Values between brackets and in parentheses indicate ranges and 95% confidence intervals, respectively.
a Adult cestodes from these species were not found.
Five cestode taxa exhibited a prevalence >10%, of which four, A. caseyi, P. auriculatum, P. armigerum and Tetraphyllidea sp., were shared among the three blue shark samples, and one, M. horridus, occurred in both Galicia and Valencia (S) (table 2). The remaining four cestode taxa were found only in Galicia (table 2). The abundance of four of the five cestode taxa with adult specimens differed significantly between host samples (table 3). The post-hoc comparison revealed that the pattern of differences was not consistent in all taxa; the abundance of P. auriculatum and P. armigerum was significantly higher in Galicia compared with Valencia (C), whereas the abundance of A. caseyi was highest and smallest in the two samples from Valencia, and that from M. horridus was significantly higher in Valencia (S) compared with the two other samples (table 3).
Table 3. Results of Kruskal–Wallis tests (H) for differences in abundance of five cestode taxa and two infracommunity descriptors between three samples (corresponding to two degrees of freedom) of blue sharks, Prionace glauca, collected from Iberian waters, captured in Galicia (n = 16) and Valencia (C) (n = 13) and stranded along the coast of Valencia (S).
The comparison of species richness and diversity are made considering all cestode taxa and only the species for which at least one adult worm was found.
In contrast, we did not detect significant differences in infracommunity species richness among the shark samples (table 3). Considering all cestode taxa, mean species richness (95% CI) was 2.69 (2.10–3.31) for Galicia, 1.75 (1.13–2.50) for Valencia (S) and 2.46 (2.00–2.92) for Valencia (C); when only species with adult specimens were selected, these figures were 2.13 (1.63–2.63), 1.63 (1.13–2.13) and 2.08 (1.72–2.39), respectively. In the case of Brillouin's diversity index, significant differences did show up only when all cestode taxa were considered, with values being 0.59 (0.41–0.78), 0.19 (0.04–0.34) and 0.50 (0.36–0.63), respectively. For the subset of cestode species with adult specimens, values of Brillouin's diversity index were 0.42 (0.27–0.56), 0.17 (0.04–0.33) and 0.43 (0.31–0.54).
Aside from the present study, we found six surveys reporting on the tapeworm fauna of the intestine of blue sharks; two and one from the North and South Pacific Ocean, respectively, two from the North Atlantic Ocean and one from the Mediterranean Sea (table 4). Overall, 11 nominal taxa were reported, and there were significant differences between the eight host samples in all of them (exact Chi-square, P < 0.05). Only one species, that is, P. auriculatum, was shared among all host samples, although with obvious differences in prevalence and mean intensity (table 4). Species of Anthobothrium (particularly A. caseyi except in one case of undetermined identity), Prosobothrium (P. armigerum or P. japonicum) were found in all but one sample, and species of Scyphophyllidium (particularly S. prionacis except in one case of undetermined identity) in all but two samples. Two other taxa, that is, Phoreiobothrium lasium and Molicola horridus, occurred more idiosyncratically (table 4). Although mean infracommunity species richness ranked from 0.69 to 3.67 spp./host, values were remarkably similar in six of the eight surveys, around 2 to 2.7 spp./host (table 4).
Table 4. Comparison of infection parameters, and species richness, of adult cestode fauna found in the intestine of blue sharks, Prionace glauca, collected all over the world.
P, prevalence; MI, mean intensity; na, information not available.
References: 1, Méndez & Galván-Magaña (Reference Méndez and Galván-Magaña2016); 2, Preti et al. (Reference Preti, MacKenzie, Spivey, Noble, Jones, Appy and Pierce2020); 3, Escalante (Reference Escalante1986); 4, Curran & Caira (Reference Curran and Caira1995); 5, Henderson et al. (Reference Henderson, Flannery and Dunne2002); 6, The current study; and 7, Euzet (Reference Euzet1959).
We found 93 records of 15 intestinal cestodes infecting blue sharks that had been identified to species level (online supplementary appendix S1). A total of seven species, including one of ‘Tetraphyllidea’ (A. caseyi), four of Onchoproteocephalidea (Pla. auriculatum, Pro. armigerum, Pro. japonicum and Phoreiobothrium sp. [=P. lasium]), and two of Phyllobothriidea (Pelichnibothrium speciosum and S. prionacis), were reported only from blue sharks. For all these species, records encompassed at least the Pacific and Atlantic/Mediterranean basins, except Phoreiobothrium sp. (=P. lasium), for which records from the Pacific Ocean were not found (fig. 1 and online supplementary appendix S1). In contrast, the eight species of Trypanorhyncha ever found in blue sharks were also reported from a wide range of elasmobranchs (from one to 19 species depending on the species), mainly of the family Carcharhinidae (online supplementary appendix S1). These species are also geographically widespread in tropical and temperate waters worldwide (fig. 1). It is important to highlight the case of the two species of Nybelinia described infecting blue sharks:. Nybelinia schmidti has only been reported also infecting shortfin mako sharks, Isurus oxyrinchus (Lamnidae); and Nybelinia pintneri infecting I. oxyrinchus and the milk shark, Rhizoprionodon acutus (Carcharhinidae).
Fig. 1. Map showing the locations where adult cestode species that can be found in the intestine of Prionace glauca have been reported (see references in online supplementary appendix S1). Blue triangles indicate the ‘core’ species found only in P. glauca (see text); circles indicate species of the Trypanorhyncha that have been described infecting P. glauca; blue circles indicate records in P. glauca; and orange circles indicate records in other hosts.
At genus level, the literature search revealed the following patterns (fig. 2 and online supplementary appendix S2): the monotypic genus Pelichnibothrium was exclusive to blue sharks, Prosobothrium (three spp.) was shared with Sphyrnidae (a single species), Anthobothrium (eight spp.) and Platybothrium (ten spp.) mostly with other Carcharhiniidae and, finally, Phoreiobothrium (18 spp.) was shared with both Sphyrnidae and Carcharhiniidae species. In the case of Scyphophyllidium (51 spp.) and most genera of the Trypanorhyncha, the bulk of species were allocated in the Carcharhinidae, but also occurred in a number of other families and orders of sharks and batoids (fig. 2 and online supplementary appendix S2). An exception was that of Molicola (three spp.), whose species only infect Lamniformes and blue sharks.
Fig. 2. Host–parasite associations of adult cestode taxa infecting the intestine of blue sharks, Prionace glauca, based on data from the literature. The phylogenetic tree of elasmobranchs (adapted from Iglésias et al. Reference Iglésias, Lecointre and Sellos2005, Naylor et al. Reference Naylor, Caira, Jensen, Rosana, Straube and Lakner2012, Amaral et al. Reference Amaral, Pereira, Silva, Amorim and de Carvalho2017), shows families of Lamniforms and Carcharhiniforms, along with the other orders of sharks and the Batoidea as a single group. Dark blue boxes indicate species specific to P. glauca, and light blue boxes indicate species also infecting other hosts (see online supplementary appendix S2). For the columns referring to other species of the cestode genera the boxes indicate number of other hosts described within the family, order or superorder: bold underlined numbers indicate the main host group (see online supplementary appendix S2). Numbers in the phylogenetic tree: 1. Lamniforms (in orange: 1.1 Alopiidae 1.2 Odontaspididae 1.3 Pseudocarchariidae 1.4 Megachasmidae 1.5 Carchariidae 1.6 Cetorhinidae 1.7 Lamnidae 1.8 Mitsukurinidae), 2. Carcharhiniformes (in blue: 2.1 Pentanchidae 2.2 Carcharhinidae 2.3 Sphyrnidae 2.4 Hemigaleidae 2.5 Leptochariidae 2.6 Triakidae 2.7 Pseudotriakidae 2.8 Proscylliidae 2.9 Scyliorhinidae), 3. Orectolobiformes, 4. Heterodontiformes, 5. Squatiniformes, 6. Pristiophoriformes, 7. Squaliformes, 8. Echinorhiniformes, 9. Hexanchiformes, 10. Batoidea.
Discussion
In this study we surveyed the intestinal parasites of blue sharks in Iberian waters, where no previous records exist. None of the taxa identified at least to genus level is new for this host species, but as many as four tapeworm taxa could only be assigned to sub-familial level at best. A potential concern is therefore, whether freezing of intestines could have damaged cestode specimens hampering a proper identification (e.g. Preti et al., Reference Preti, MacKenzie, Spivey, Noble, Jones, Appy and Pierce2020). We are aware that freezing of organs is not recommended for taxonomic work on helminths, especially when dealing with delicate forms such as tapeworms. However, sampling of large sharks is often opportunistic and subject to trade-off with the stakeholders (fishers and staff of stranding networks). Perhaps not surprisingly, other parasitological surveys on blue sharks have also dealt with frozen samples (Henderson et al., Reference Henderson, Flannery and Dunne2002; Preti et al., Reference Preti, MacKenzie, Spivey, Noble, Jones, Appy and Pierce2020). Fortunately, the tapeworms from this study that could only be assigned to coarse taxonomic groups contained just immature specimens lacking diagnostic traits and for which the blue shark are putative non-hosts. We interpret that these immature forms are likely specific to other elasmobranchs and do not reproduce in blue sharks; thus, they could be considered as accidental parasites such as, for example, Anisakis spp. are in other sharks (Penadés-Suay et al., Reference Penadés-Suay, Tomás, Merchán and Aznar2017). The degree of preservation of samples of the remaining tapeworm taxa, all containing adults, allowed reliable specific identifications (see below) except for Scyphophyllidium sp. for which a single scolex could be collected. In any event, the voucher specimens deposited at the Natural History Museum of London will afford researchers further taxonomic re-examination, if necessary, for example, via molecular markers.
The ‘true’ tapeworm communities of blue sharks in Iberian waters were thus composed of four to five species (depending on whether Scyphophyllidium sp. is included). Three species were common to the three host samples analysed, being cosmopolitan parasites specific to blue sharks (online supplementary appendix S1). Anthobothrium caseyi can be differentiated from other congeneric species by their proglottid laciniations, which are approximately as long as wide (Ruhnke & Caira, Reference Ruhnke and Caira2009); Pla. auriculatum, by the acutely recurved base of the medial hook on the scolex (see Healy, Reference Healy2003); and Pro. armigerum by its scolex formed by four glandular sessile discs (Khalil et al., Reference Khalil, Jones and Bray1994). Two other cosmopolitan species of the order Phyllobothriidea have been reported exclusively in blue sharks, Scyphophyllidium prionacis and Pelichnibothrium speciosum (online supplementary appendix S1), but none of them were verified in this study. The scolex of the specimen assigned to Scyphophyllidium sp. superficially resembled that of S. prionacis but was in a very poor state of conservation, and the lack of proglottids precluded an unequivocal identification. Finally, we detected specimens of M. horridus in two of the three shark samples. This species had previously been detected in blue sharks from other Atlantic and Mediterranean localities (online supplementary appendix S1), and can be told from other species of the genus by its sequence of 8–10 macrohooks at the base of the tentacles (Palm, Reference Palm2004).
Little geographical signal emerged when we compared the tapeworm assemblages of Atlantic and Mediterranean blue shark samples. This would be at odds with recent evidence showing certain degree of potential isolation of Mediterranean blue shark populations (Leone et al., Reference Leone, Urso, Damalas and Martinsohn2017). First, there were not obvious differences in species composition at component community level. Even if we assume that the specimen of Scyphophyllidium collected in Galicia actually is a ‘true’ member of the community, that is, S. prionacis, its absence in the Mediterranean samples could hardly result from a true biogeographical gap, since Euzet (Reference Euzet1959) reported S. prionacis in other localities from the western Mediterranean with high prevalence. Second, the geographical comparison of species richness or diversity at infracommunity level failed to be significant. Admittedly, the power of tests was low because host sample sizes were small, but we did detect significant differences when looking at infection parameters of most cestode species. However, these individual differences do not show a consistent geographical pattern.
Sampling heterogeneity could have blurred any potential geographical signal. For instance, M. horridus exhibited the highest infections in the Valencia (S) sample, which contained the largest, and presumably oldest, blue shark specimens; infections were intermediate in Galicia, which included a combination of both juvenile and adult sharks; and this parasite did not appear in the Valencia (C) sample, which was composed only of juveniles. It is therefore tempting to suggest that the host size/age influenced the likelihood of infection with M. horridus. In fact, this parasite has been reported as plerocercoid in the liver of large pelagic teleosts, including the sunfish, Mola mola, and swordfish, Xiphias gladius (e.g. Palm, Reference Palm2004; Fernández et al., Reference Fernández, Oyarzún, Valenzuela, Burgos, Guaquín and Campos2016; Ahuir-Baraja et al., Reference Ahuir-Baraja, Yamanoue and Kubicek2017), which are prey of large blue sharks (e.g. Bornatowski & Schwingel, Reference Bornatowski and Schwingel2008; Pope et al., Reference Pope, Hays and Thys2010; Markaida & Sosa-Nishizaki, Reference Markaida and Sosa-Nishizaki2010) but that can hardly be consumed by juvenile sharks. Similar changes in parasite abundance (both positive and negative) with host length have been reported in other shark species and seem to be clearly linked to ontogenetic dietary shifts (Randhawa & Brickle, Reference Randhawa and Brickle2011).
In any event, inter-sampling heterogeneity in infection levels has not only been observed in this study, it is indeed a salient feature of our broad-scale geographical comparison. We observed that infracommunity species richness tended to be similar across localities, but infection levels of all cestode species showed significant, sometimes extreme variations. As expressed by Henderson et al. (Reference Henderson, Flannery and Dunne2002), this variability seems inevitable because infection rates are determined by a multitude of biotic and abiotic factors. Of particular significance are the local differences in the diet of blue sharks (see, e.g. references in Markaida & Sosa-Nishizaki, Reference Markaida and Sosa-Nishizaki2010; Loor-Andrade et al., Reference Loor-Andrade, Pincay-Espinoza and Rosas-Luis2017), and in the number of intermediate/paratenic hosts available. Cephalopods and teleosts are the key prey groups of blue sharks (Markaida & Sosa-Nishizaki, Reference Markaida and Sosa-Nishizaki2010; Hernández-Aguilar et al., Reference Hernández-Aguilar, Escobar-Sánchez, Galván-Magaña and Abitia-Cárdenas2016; Córdova-Zavaleta et al., Reference Córdova-Zavaleta, Mendo, Briones-Hernandez, Acuna-Perales, Gonzalez-Pestana, Alfaro-Shigueto and Mangel2018) and both types of prey have also been reported as hosts for larvae of Anthobothrium spp. (Dollfus, Reference Dollfus1923; Jensen & Bullard, Reference Jensen and Bullard2010; Schwerdt, Reference Schwerdt2015; Tedesco et al., Reference Tedesco, Caffara, Gustinelli, Fiorito and Fioravanti2020); Prosobothrium spp. (Avdeeva, Reference Avdeeva1989; Williams & Bunkley-Williams, Reference Williams and Bunkley-Williams1996; González & Kroeck, Reference Gonzalez and Kroeck2000); and Scyphophyllidium spp. (Gaevskaya & Schuhgalter, Reference Gaevskaya and Schuhgalter1992; Schuhgalter, Reference Schuhgalter1992; Jensen & Bullard, Reference Jensen and Bullard2010). However, it is not possible to morphologically identify the larval stages to species level, except for the Trypanorhyncha (Palm, Reference Palm2004; Palm & Caira, Reference Palm and Caira2008) and, therefore, this precluded a quantitative assessment of the potential communities of intermediate/paratenic hosts at a local or even regional scale. In this context it is worth mentioning that as many as one-quarter of species for the Trypanorhyncha seem to use only one to two prey species as intermediate/paratenic hosts (Palm & Caira, Reference Palm and Caira2008). Accordingly, local variation in the consumption of these prey can generate dramatic differences in the infection rates of the definitive host.
At a global geographical scale, tapeworm communities of blue sharks were composed of approximately ten cestode taxa, seven of which (those belonging to the Phyllobothriidea, Onchoproteocephalidea and ‘Tetraphyllidea’) are exclusive to this host species, corroborating the general pattern of specificity observed for these orders (Caira & Jensen, Reference Caira and Jensen2014). These exclusive species share two fundamental traits. First, they appear to have a cosmopolitan distribution as their host species. The only exception is the enigmatic Phoreiobothrium sp., which has apparently only been referred to in an article from the Mediterranean (Euzet, Reference Euzet1959). The species was identified as P. lasium, but re-examination of the specimens suggests that it is an exclusive species infecting blue sharks yet to be described (Euzet, Reference Euzet1959; Caira et al., Reference Caira, Richmond and Swanson2005). Second, all the cestode species unique to blue sharks belong to genera whose bulk diversity appears in carcharhinids with diverse ecologies.
These patterns would suggest that a group of cestode species has geographically accompanied’ the blue sharks with apparently little diversification (with perhaps the exception of P. japonicum in the Pacific Ocean). As noted above, blue sharks are highly migratory and exhibit limited genetic structure across populations sampled from disparate oceanic regions (Madigan et al., Reference Madigan, Shipley, Carlisle, Dewar, Snodgrass and Hussey2021). Accordingly, this pool of tapeworm species would potentially appear, in any sampling location, with greater or lesser prevalence and intensity, thus providing similarity to infracommunity composition and diversity, such as observed. The additional occurrence of trypanorhynchan cestodes in these communities would be less predictable depending on both the composition of the local elasmobranch community and the patterns of cestode exchange through the food web. Conversely, the quantitative differences in tapeworm faunas across localities would result from: (a) the variability of the local transmission rate of each cestode species (which, in part, would depend on the host diet and the density of intermediate/paratenic hosts); and (b) the mobility of blue sharks with respect to the life span of the parasites. This factor is important because satellite tracking data indicate that blue sharks can travel thousands of kilometres in a few months (Vandeperre et al., Reference Vandeperre, Aires-da-Silva, Fontes, Santos, Serrão Santos and Afonso2014; Kai & Fujinami, Reference Kai and Fujinami2020). Indeed, in the Atlantic Ocean, long-term tagging data indicate such an extensive range of movements that the whole population of blue sharks are considered as a single stock (Kohler & Turner, Reference Kohler and Turner2019). This suggests that parasites acquired in a specific region could be transported to very remote sampling areas, thus contributing, at first glance, to homogenize parasite assemblages. Nevertheless, the persistence of the carried parasites in these areas would depend on the local occurrence of appropriate intermediate hosts to guarantee the completion of life-cycles; otherwise, the parasites would gradually be lost (see, e.g. Torchin et al., Reference Torchin, Lafferty, Dobson, McKenzie and Kuris2003; Diamant, Reference Diamant, Golani and Appelbaum-Golani2010).
As a final remark it is interesting to note that, for the cestode order with a more broad-based pattern of host preference, that is, the Trypanorhyncha, there are two putative instances of host-switching, that is, Molicola horridus and Nybelinia schmidti. Both species reproduce in two phylogenetically unrelated hosts, that is, the blue shark and the shortfin mako shark, two cosmopolitan species which share prey in a common oceanic habitat. It is interesting to put the overall specificity patterns of tapeworms from blue sharks in a broader context. In a recent study, Beer et al. (Reference Beer, Ingram and Randhawa2019) found a substantial number of co-speciation events among tapeworm assemblages in skates, leading to narrow specificity to single host species. Indeed, this might be the case for the ‘core’ tapeworm species that have exclusively been reported in blue sharks; note, however, that the narrow specificity of many tapeworms from elasmobranchs does not necessarily imply strict co-speciation (Caira & Jensen, Reference Caira and Jensen2001). On the other hand, Beer et al. (Reference Beer, Ingram and Randhawa2019) also detected that a combination of ecological factors (inter alia, host size and diet) could account for a non-negligible number of host-switching events in the skate-tapeworm associations they studied, similarly as noted here for M. horridus and N. schmidti in blue sharks. Thus, a salient point that can be drawn from this evidence is that, for blue sharks, and probably other elasmobranchs, the influence of ecological factors upon their tapeworm communities is idiosyncratic and also constrained by historical factors, that is, the strong host specificity of most of their tapeworm species. Such ‘Gleasonian’ features could explain why only a few generalizations have been found on the ecological factors that provide structure to tapeworm communities of sharks (Randhawa & Poulin, Reference Randhawa and Poulin2010; Rasmussen & Randhawa, Reference Rasmussen and Randhawa2018).
Supplementary material
To view supplementary material for this article, please visit https://doi.org/10.1017/S0022149X22000803
Acknowledgements
Samples of sharks for this study from Galicia were made possible thanks to an agreement between ‘Asociación Chelonia’ and the port of Vigo and its fishermen association; we would like to thank them all for their support. We specially thank Manuel Merchán and Antonio Castro, along with other members of Chelonia, for their assistance in sampling and logistics. Stranded sharks could be obtained thanks to the assistance of the Stranding Network for Cetaceans and Marine Turtles of the Valencian Community, which is supported by the Environmental Service (Dirección General del Medio Natural) of the Valencian Government (Generalitat Valenciana). Samples from the Valencia fishing fleet would have not been possible without the unconditional collaboration of Captain Juan Pedro.
Financial support
This work was supported by project AICO/2021/022, Generalitat Valenciana, Spain.
Conflicts of interest
None.
Ethics statement
The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional guides on the care and use of laboratory animals, as samples were obtained from commercial captures or stranded animals.
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