- Email: [email protected]
Cestodes from deep-water squaliform sharks in the Azores
Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
Contents lists available at ScienceDirect
Deep-Sea Research II journal homepage: www.elsevier.com/locate/dsr2
Cestodes from deep-water squaliform sharks in the Azores Janine N. Caira, Maria Pickering n Department of Ecology & Evolutionary Biology, 75 N. Eagleville Road, Unit 3043, University of Connecticut, Storrs, CT 06269-3043, USA
art ic l e i nf o
Keywords: Azores Cestodes Condor seamount Deep-water sharks Tapeworms
a b s t r a c t The majority of our knowledge on marine tapeworms (cestodes) is limited to taxa that are relatively easy to obtain (i.e., those that parasitize shallower-water species). The invitation to participate in a deepwater research survey off the Condor seamount in the Azores offered the opportunity to gain information regarding parasites of the less often studied sharks of the mesopelagic and bathypelagic zone. All tapeworms (Platyhelminthes: Cestoda) found parasitizing the spiral intestine of squaliform shark species (Elasmobranchii: Squaliformes) encountered as part of this survey, as well as some additional Azorean sampling from previous years obtained from local fishermen are reported. In total, 112 shark specimens of 12 species of squaliform sharks representing 4 different families from depths ranging between 400 and 1290 m were examined. Cestodes were found in the spiral intestines from 11 of the 12 squaliform species examined: Deania calcea, D. cf. profundorum, D. profundorum, Etmopterus princeps, E. pusillus, E. spinax, Centroscyllium fabricii, Centroscymnus coelolepis, C. cryptacanthus, C. crepidater, and Dalatias licha. No cestodes were found in the spiral intestines of Centrophorus squamosus. Light microscopy and scanning electron microscopy revealed several potentially novel trypanorhynch and biloculated tetraphyllidean species. Aporhynchid and gilquiniid trypanorhynchs dominated the adult cestode fauna of Etmopterus and Deania host species, respectively, while larval phyllobothriids were found across several host genera, including, Deania, Centroscyllium, and Centroscymnus. These results corroborate previous findings that deep-water cestode faunas are relatively depauperate and consist primarily of trypanorhynchs of the families Gilquiniidae and Aporhynchidae and larval tetraphyllideans. A subset of specimens of most cestode species was preserved in ethanol for future molecular analysis to allow more definitive determinations of the identification of the larval tetraphyllideans and trypanorhynchs lacking evaginated tentacles and other key diagnostic features. & 2013 Elsevier Ltd. All rights reserved.
1. Introduction Our understanding of the tapeworms that parasitize many of the world's 1200 species of sharks and rays (i.e., elasmobranchs, see Naylor et al., 2012a, 2012b) has expanded considerably over the past two decades (e.g., see Jensen, 2005; Palm, 2004; Ruhnke, 2011; Tyler, 2006). This work has placed particular emphasis on hosts occupying epibenthic and epipelagic habitats (i.e., depths of r200 m) in large part because animals inhabiting these relatively shallow waters are readily accessible and easily procured in collaboration with artisanal fishing enterprises. This is not, however, the case for deeper water elasmobranchs, and sharks in particular. With respect to the two most speciose groups of deepwater sharks (i.e., Squaliformes and Scyliorhinidae), in the most recent comprehensive synopsis of the metazoan parasites of deepwater fishes of the world, Klimpel et al.'s (2001) checklist included
n
Corresponding author. Tel.: þ 1 805 637 6180; fax: þ 1 860 486 6364. E-mail addresses: [email protected] (J.N. Caira), [email protected] (M. Pickering).
cestode (tapeworm) data for only 12 of the 121 species of dogfish sharks (Squaliformes) and only 1 of the 154 species of catsharks (Scyliorhinidae) listed by Compagno et al. (2005). This checklist reveals that the majority of cestodes found parasitizing deepwater hosts consist of larval cestodes in the order Tetraphyllidea and adult cestodes of the order Trypanorhyncha. Although Palm (2004) expanded trypanorhynch cestode records to include 27 species of squaliform hosts and 6 species of scyliorhinid hosts, the tapeworm faunas of the majority of species of deep-water sharks are completely unknown. The Condor seamount project provided an invaluable opportunity for us to expand knowledge of tapeworms of deeper water sharks, and squaliforms in particular. Some of the sharks examined for the purposes of this study had never previously been examined for cestodes; most had never been examined in this region. In fact, to our knowledge, existing data for adult cestodes from deepwater sharks in the vicinity of the Azores come primarily from M.S. (e.g., Schröder, 1999) and Ph.D. (e.g., Noever, 2009) theses, only a subset of the results of which have been formally published (e.g., Palm and Schröder, 2001), in the latter case for the Great
0967-0645/$ - see front matter & 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.dsr2.2013.08.008
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
J.N. Caira, M. Pickering / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
2
Meteor Bank in the central northeast Atlantic, 1000 km south of the Azores. Guiart's (1935) report of cestodes from deep-water sharks in the Azores includes only larvae. Our goal here is to provide preliminary identifications and basic morphological data using scanning electron microscopy and/or light microscopy for the cestode taxa found parasitizing the squaliform shark species examined over the course of the surveys. With the exception of Noever et al. (2010) formal descriptions of the novel tapeworm taxa encountered during this study have yet to be generated and will be published separately, as will the results of analyses conducted on specimens of each tapeworm species preserved for the generation of molecular data. To aid future work we have provided images of most cestode taxa encountered and have deposited representative voucher material in the Lawrence R. Penner Parasitology Collection, University of Connecticut, Storrs, Connecticut, United States. It is our hope that the preliminary morphological identifications provided here can be addressed using molecular data in the near future.
2. Materials and methods Sharks collected in May 2006, January 2009, and October 2012 off Faial Island, Azores resulted in a total of 112 individuals of 12 species of deeper water sharks being examined for cestodes. Specimens in 2006 and 2009 were obtained from local fishermen, which were caught as by-catch on longlines. In 2012 sharks were obtained from longline fish surveys conducted by the University of the Azores on the R.V. Arquipélago in conjunction with the Condor seamount studies (Giacomello et al., this issue), and were collected at depths between 400 m and 1290 m around the Condor seamount between 38141'43″N, 29120'12″W and 38131'24″N, 28159'30″W. Data reported here are for all squaliform taxa examined. With two exceptions host identities and family-level classification follow Naylor et al. (2012a, 2012b). Specimens examined were as follows: Centrophoridae: 4 Centrophorus squamosus, 13 Deania calcea, 1 Deania profundorum, and 1 Deania cf. profundorum (sensu Naylor et al., 2012b); Etmopteridae: 11 Etmopterus princeps, 15 Etmopterus pusillus, 23 Etmopterus spinax, and 6 Centroscyllium fabricii; Somniosidae: 14 Centroscymnus coelolepis, 7 Centroscymnus cryptacanthus (treated as Centroscymnus owstonii by Naylor et al., 2012a, 2012b), and 10 Centroscymnus crepidater (treated as Centroselachus crepidater by Naylor et al., 2012a, 2012b); Dalatiidae: 7 Dalatias licha. Additional details regarding sex, size, and depth of collection for all shark species are provided in Table 1. The specific identity of 30 of the 112 specimens was verified in the molecular analysis of the NADH2 gene
in Naylor et al. (2012b). Voucher tissue samples preserved in 95% ethanol were taken from all 112 specimens; photographs of each shark were also taken. The unique host specimen identification numbers of infected individuals (collection code “AZ” followed by collection number) are provided in relevant sections below, and correspond to those used in Naylor et al. (2012b). Images of most specimens and detailed collection and demographic data of all specimens can be accessed at the following URL: www.elasmobranchs.tapewormdb.uconn.edu by entering the collection code AZ and the appropriate collection number. Data presented are for taxa parasitizing the spiral intestine only. The spiral intestine of each shark was opened with a mid-ventral longitudinal incision, and was examined for cestodes under a stereomicroscope. Cestodes found were preserved in either 95% ethanol for future molecular work or 4% seawater buffered formalin for further morphological examination. The spiral intestines were then fixed in 4% seawater buffered formalin for approximately a week and then transferred to 70% ethanol for long-term storage and further study. Preparations of cestodes as whole mounts and for examination with scanning electron microscopy (SEM) followed standard protocols (e.g., Pickering and Caira, 2008; Rodriguez et al., 2011). Museum abbreviations used are as follows: IPCAS, Institute of Parasitology, Academy of Sciences of the Czech Republic, České Budĕjovice, Czech Republic; LRP, Lawrence R. Penner Parasitology Collection, University of Connecticut, Storrs, Connecticut, United States; MHNFCUP, Museu de História Natural da Faculdade de Ciências da Universidade do Porto, Porto, Portugal; USNPC, United States National Parasite Collection, Beltsville, Maryland, United States. Larval cestode terminology follows Chervy (2002); microthrix terminology follows Chervy (2009). Trypanorhynch classification follows Palm (2004) and Olson et al. (2010).
3. Results In total, 48 (i.e., 43%) of the 112 squaliform sharks examined were found to host cestodes of any life cycle stage (i.e., larva, juvenile, or adult) in their spiral intestine (see Table 1); 35.7% hosted juvenile or adult cestodes. The overall prevalence of infection with cestodes in each species of shark ranged from 0% (Centrophorus squamosus) to 73.9% (Etmopterus spinax). Infections ranged from 1 to 3 cestode species per infected shark. The average number of cestode species (regardless of life cycle stage) found per shark species was 1.75 worm species; excluding larval stages, the average was 1.17. However, as noted below in the
Table 1 Detail of squaliform shark species examined for cestodes and number infected by sex. Shark species
Centrophoridae Centrophorus squamosus Deania calcea Deania cf. profundorum Deania profundorum Dalatiidae Dalatias licha Etmopteridae Centroscyllium fabricii Etmopterus princeps Etmopterus pusillus Etmopterus spinax Somniosidae Centroscymnus coelolepis Centroscymnus owstonii Centroselachus crepidater
Total no. examined
Depth collected (m)
Shark total length (cm)
No. examined (No. infected) females
No. examined (No. infected) males
4 13 1 1
1090–1265 1090–1265 540 451–500
121–129 81–112 95 41
4 (0) 10 (6) 1 (1) 1 (1)
– 3 (0) – –
401–540
114.5–123
–
7 (4)
6 11 15 23
1260–1290 1090–1290 500–850 540–750
57–81.5 48–69.5 24.5–48.5 30–43
5 (1) 7 (0) 7 (2) 22 (16)
1 4 8 1
14 7 10
1090–1290 1090–1265 1051–1265
85–118.5 84.5–114 61–84.5
6 (5) 6 (3) 8 (2)
8 (4) 1 (0) 2 (0)
7
(0) (1) (1) (1)
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
J.N. Caira, M. Pickering / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
detailed data provided for each species, species counts presented are conservative. In several instances it is possible that diversity has been underestimated, and further scrutiny is required to confirm these numbers. A total of 3 to 4 larval cestode species was encountered across the 12 squaliform species examined. In addition, 1–2 juvenile cestode taxa and 12–14 adult cestode species were collected. In the sections that follow, the cestode faunas encountered are treated separately for each of the 12 shark species, which are presented according to shark family group. Unfortunately, definitive identification of many of these cestodes based solely on morphology was hampered by the following: (1) in most cases the number of specimens collected was small, (2) most trypanorhynchs lacked everted tentacles and thus also the diagnostic characteristics required for specific identification, and (3) most tetraphyllideans were either larval or juvenile individuals that lacked the diagnostic proglottid features of these taxa. The adult cestode species that we were able to definitively identify were new to science and have already been formally described (see Noever et al., 2010). We have presented scanning electron micrographs here of as many of the remaining taxa as possible in order to facilitate their future identification.
3.1. Centrophoridae (Gulper Sharks) 3.1.1. Centrophorus squamosus None of the 4 individuals examined was found to host cestodes.
3.1.2. Deania calcea (Infected: AZ-108, AZ-111, AZ-112, AZ-131, AZ-132, AZ-152) Six of the 13 individuals (46.2%) examined hosted cestodes. Five of these hosted specimens of Deanicola Beveridge, 1990. With respect to the 2 known species in this genus, these specimens lack the conspicuous pars post-bulbosa of D. protentus Beveridge, 1990 and we believe they represent 2 distinct species of Deanicola. One (Figs. 1–7; LRP 8063–8085) is generally consistent with D. minor Beveridge, 1990. The second is more robust and at least some specimens exhibit a substantially greater number of testes and we believe potentially represents a new species referred to here as Deanicola sp. 1 (Figs. 8–12; LRP 8086–8107). Given the low number and condition of the specimens we are unable to present prevalence data separately for the 2 forms. SEM reveals that the scoleces of both species bear palmate spinitriches with 13 digits on their proximal surfaces (Figs. 3 and 10), 20 or more digits on the anterior of peduncle (Fig. 5), and 16 digits on the posterior surfaces of the peduncle (Figs. 6 and 11). The spinitriches found on the distal bothrial surfaces are pectinate and bear 5–6 digits (Figs. 4 and 12). The apex of the scolex (Fig. 2) and the distal bothrial surfaces also bear capilliform filitriches; the proximal bothrial surfaces also bear acicular filitriches. Specimens of both forms of Deanicola were preserved in 95% ethanol for future molecular work; the hologenophores of these specimens have been deposited in LRP (8151–8152 for D. minor; 8153 for Deanicola sp. 1). D. calcea also hosted what appear to be two forms of larval tetraphyllidean cestodes. Three sharks hosted plerocercoids (LRP 8108–8113) that bear a close resemblance to Clistobothrium montaukensis Ruhnke, 1993. Two different sizes of this larval stage were found. It is possible that the smaller form (Fig. 21) is merely a younger stage of the larger form (Fig. 22). One shark hosted a plerocercoid (Fig. 23) with a scolex that bears a strong resemblance to the phyllobothriid Clistobothrium carcharodoni Dailey and Vogelbein, 1990.
3
3.1.3. Deania cf. profundorum (Infected: AZ-46) The single specimen of this species examined, which we note based on the results of Naylor et al. (2012b) is not conspecific with Deania profundorum, hosted specimens of a small typanorhynch that appears to belong to the genus Deanicola (LRP 8154–8165). All are immature, but it appears to represent a species different than those seen in D. calcea. 3.1.4. Deania profundorum (Infected: AZ-161) The single specimen of this shark species examined hosted 1 specimen of what appears to be a juvenile of the trypanorhych genus Aporhynchus Nybelin, 1918 (LRP 8148). Its juvenile form makes definitive identification of this specimen impossible at this time. However, it was preserved in 95% ethanol and thus its identity may be confirmed in the future using molecular data. 3.2. Etmopteridae (Lantern Sharks) 3.2.1. Etmopterus princeps (Infected: AZ-104) Only 1 of the 11 individuals (9%) of this species examined was infected. This single shark hosted specimens of 3 species of trypanorhynchs. These include what we believe is a new species of Gilquinia (Figs. 13–18; LRP 8114–8118). Unfortunately, no specimens were found with their tentacles everted. With respect to the 3 known members of this genus, it possesses a greater number of testes than G. stevensi Beveridge, 1990 and fewer testes than G. squali (Fabricius, 1794) Dollfus, 1930 (i.e., 219 vs. 87–108 and 278–348, respectively). The pattern of microtriches on its scolex differs conspicuously from that reported for the third member of the genus, G. robertsoni Beveridge, 1990, by Palm (2004; Figs. 79a–f). SEM shows our specimens to bear acicular filitriches and no spinitriches on the peduncular (Fig. 15) and proximal bothrial (Fig. 16) surfaces, and spathulate spinitriches and capilliform filitriches on its interbothrial (Fig. 17) and distal bothrial (Fig. 18) surfaces. This shark also hosted a single immature specimen of what we believe represents a species of Aporhynchus (LRP 8119). In addition, several specimens that resemble Plesiorhynchus brayi Palm, 2004 reported by Palm (2004), also from the North Atlantic, in overall morphology (Figs. 19 and 20; LRP 8120) were found. 3.2.2. Etmopterus pusillus (Infected: AZ-50, AZ-51, AZ-147) Only 3 of the 15 individuals (20%) of this species examined were infected. These sharks each hosted a few specimens of the new aporhynchid trypanorhynch, Aporhynchus pickeringae Noever, Caira, Kuchta, Desjardins, 2010, the description of which has already been formally communicated (see Noever et al., 2010). The specimens of this species were deposited in museums as follows: Holotype (MHNFCUP no. 078883); scoleces of juveniles of 2 paratypes (USNPC nos. 103217–103218), partial strobilae of 2 paratypes (USNPC nos. 103219–103220); scoleces of juveniles of 2 paratypes (LRP no. 7365), partial strobila of 1 paratype (LRP no. 7364); free proglottid of 1 paratype (IPCAS no. 560). 3.2.3. Etmopterus spinax (Infected: AZ-1, AZ-2, AZ-5, AZ-6, AZ-7, AZ-8, AZ-9, AZ-44, AZ-65, AZ-68, AZ-71, AZ-74, AZ-75, AZ-76, AZ-77, AZ-78, AZ-150) A total of 17 of the 23 specimens (i.e., 73.9%) examined were infected. One shark hosted a single specimen of Aporhynchus norvegicus (USNPC 103221). All 17 sharks hosted juvenile and/or adult specimens of the new aporhynchid trypanorhynch Aporhynchus menezesi Noever, Caira, Kuchta, Desjardins, 2010 the description of which has also already been published (see Noever et al., 2010). The specimens of this species were deposited in museums as follows: Holotype (MHNFCUP no. 078882) and 1 paratype (MHNFCUP no.
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
4
J.N. Caira, M. Pickering / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
Fig. 1–12. Scanning electron micrographs of Deanicola minor and Deanicola sp. 1 cestodes found parasitizing Deania calcea. (1) Scolex of Deanicola minor; scale bar, 100 mm. Note: small numbers correspond to Figs. 2–6, 10–12 showing higher magnification images of these surfaces. (2) Apical surface of scolex in D. minor; scale bar, 2 mm. (3) Proximal surface of scolex in D. minor; scale bar, 2 mm. (4) Distal surface of scolex in D. minor; scale bar, 2 mm. (5) Anterior surface of peduncle in D. minor; scale bar, 100 mm. (6) Posterior surface of peduncle in D. minor; scale bar, 100 mm. (7) Tentacle hooks from D. minor; scale bar, 20 mm. (8) Scolex of Deanicola sp. 1; scale bar, 100 mm. (9) Tentacle hooks from Deanicola sp. 1; scale bar, 20 mm. (10) Proximal surface of scolex in Deanicola sp. 1; scale bar, 2 mm. (11) Peduncle surface of scolex in Deanicola sp. 1; scale bar, 2 mm. (12) Distal surface of scolex in Deanicola sp. 1; scale bar, 2 mm.
078884); 1 paratype (IPCAS no. C–560); 3 paratypes (USNPC no. 103216); 1 paratype (LRP no. 7366), cross sections of terminal proglottid of 1 paratype and its strobilar voucher (LRP nos. 7374–7382), cross sections of scolex of paratype (LRP nos. 7370–7373), 3 paratypes prepared for SEM and their strobilar vouchers (LRP nos. 7367–7369), 2 egg preparations (LRP nos. 7383–7384); 3 juvenile specimens (LRP nos. 7385–7387). In addition, one specimen of a juvenile tetraphyllidean was found and saved in ethanol for future molecular analysis and identification.
3.2.4. Centroscyllium fabricii (Infected: AZ-106) Only one of the 6 individuals (17.7%) of this species was infected and this infection consisted of only a single cestode specimen (LRP 8121). We believe it belongs to the genus Gilquinia,
but given that its tentacles are retracted this identification requires confirmation. 3.3. Somniosidae (Sleeper Sharks) 3.3.1. Centroscymnus coelolepis (Infected: AZ-84, AZ-85, AZ-86, AZ-87, AZ-114, AZ-115, AZ-125, AZ-126, AZ-133) Nine of the 14 specimens (i.e., 64.3%) of this species examined hosted cestodes. All 9 hosted immature or adult specimens of a phyllobothriid tetraphyllidean bearing biloculated bothridia. Despite the fact that a number of these specimens are fully mature, we are unable to confidently place them in a known genus at this time. Among the phyllobothriid genera considered valid by Ruhnke (2011), they most closely resemble Monorygma Diesing, 1863 but lack the posterior lateral projections on the
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
J.N. Caira, M. Pickering / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
5
Fig. 13–20. Scanning electron micrographs of Gilquinia sp. 1 and Plesiorhynchus sp. cestodes found parasitizing Etmopterus princeps. (13) Scolex of Gilquinia sp. 1; scale bar, 500 mm. Small number indicates location of detail shown in Fig. 15. (14) Scolex proper of Gilquinia sp. 1; scale bar, 200 mm. Small number indicates location of detail shown in Figs. 16–18. (15) Peduncle surface of Gilquinia sp. 1; scale bar, 2 mm. (16) Proximal surface of Gilquinia sp. 1; scale bar, 2 mm. (17) Surface between bothria of Gilquinia sp. 1; scale bar, 2 mm. (18) Distal surface of Gilquinia sp. 1; scale bar, 2 mm. (19) Scolex of Plesiorhynchus sp.; scale bar, 500 mm. (20) Scolex proper of Plesiorhynchus sp.; scale bar, 200 mm.
anterior loculus seen in members of this genus. Both a smaller (Fig. 25; LRP 8122–8127) and larger (Fig. 27; LRP 8128–8135) form of this taxon was encountered and it is possible they represent different species. The bothridia of the scoleces of both forms were covered with small gladiate spinitriches on all surfaces (Fig. 26). Specimens of both forms were preserved in 95% ethanol for future molecular work. Until these taxonomic issues can be resolved we have combined data for both forms. One shark also hosted specimens of plerocercoids (LRP 8149–8150) resembling Clistobothrium montaukensis like those seen in Deania calcea.
hosted plerocercoids resembling those of C. montaukensis like those seen in D. calcea (LRP 8136). One shark hosted a merocercoid (LRP 8137) like that seen in C. coelolepis. 3.3.3. Centroscymnus crepidater (¼Centroselachus crepidater of Naylor et al., 2012a, 2012b) (Infected: AZ-122, AZ-144) Only 2 of the 10 individuals (i.e., 20%) of this species examined were infected. Both (Fig. 24; LRP 8138) hosted plerocercoids resembling C. montaukensis like those seen in D. calcea. 3.4. Dalatiidae (Kitefin Sharks)
3.3.2. Centroscymnus cryptacanthus ( ¼Centroscymnus owstonii of Naylor et al. 2012a, 2012b) (Infected: AZ-129, AZ-142, AZ-143) Three of the 7 individuals (i.e., 42.9%) of this species examined were infected, but in all cases only with larval forms. Two sharks
3.4.1. Dalatias licha (Infected: AZ-3, AZ-79, AZ-160, AZ-163) Four of the 7 individuals (i.e., 57.1%) examined were found to host cestodes. All 4 hosted numerous mature and gravid proglottids
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
6
J.N. Caira, M. Pickering / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
Fig. 21–27. Scanning electron micrographs of larval tetraphyllidean cestodes found in spiral intestines of squaliform sharks. (21) Smaller form resembling Clistobothrium montaukensis from Deania calcea; scale bar, 200 mm. (22) Larger form resembling Clistobothrium montaukensis from Deania calcea; scale bar, 500 mm. (23) Specimen resembling Clistobothrium carcharodon from Deania calcea; scale bar, 200 mm. (24) Specimen resembling Clistobothrium montaukensis from Centroscymnus crepidater; scale bar, 500 mm. (25) Scolex of smaller form of unidentified biloculate tetraphyllidean genus from Centroscymnus coelolepis; scale bar, 200 mm. Small number indicates location of detail shown in Fig. 26. (26) Distal surface of unidentified biloculate tetraphyllidean genus from Centroscymnus coelolepis; scale bar, 1 mm. (27) Scolex of larger form of unidentified biloculate tetraphyllidean genus from Centroscymnus coelolepis; scale bar, 500 mm.
(LRP 8139–8146) that are easily identified as Bilocularia hyperapolytica Obersteiner, 1914. One shark also hosted a small juvenile worm with no proglottids (LRP 8147) but bearing a scolex with 4 biloculated bothridia. This worm resembles the hyperapolytic form of B. hyperapolytica reported and illustrated by Obersteiner (1914). Euzet (1994) considered Bilocularia Obersteiner, 1914 to be a genus inquirendum as it had not been reported from its type host “Centrophorus granuluosus” since its original description. However, Williams (1958) reported finding numerous proglottids of this species in the single specimen of D. licha (as Scymnus licha) he examined off the British Isles. Williams found no scoleces, but noted that the proglottids were strikingly similar to those illustrated by Obersteiner (1914). Our results confirm D. licha as an appropriate host for this species and lead us to speculate that the identity of the type host may have been in error.
4. Discussion Infection data for the 12 species of deep-water sharks examined here are summarized in Fig. 28 by ocean zone of capture. However, it should be noted that all 12 species are known to occur in both meso- and bathyal zones (Compagno et al., 2005; Froese and Pauley, 2013). Regardless of sample size, with the exception of C. squamosus, one or more species of cestode was found parasitizing the spiral intestine of all shark species collected. Previous work on parasites of deeper water sharks (e.g., Campbell, 1983) leads us to believe that within ocean zones these infections are more likely to have occurred in benthic rather than in pelagic situations. This is because the complex life-cycles of cestodes rely on trophic transmission among hosts and the number and diversity of potential intermediate hosts is generally greater in benthic, or at
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
J.N. Caira, M. Pickering / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
7
Fig. 28. Summary of spiral intestine cestode data by ocean zone of capture for the 12 deep-water shark species examined here. Shark families are indicated as follows: (C) Centrophoridae; (D) Dalatiidae; (E) Etmopteridae; (S) Somniosidae.
least demersal, habitats than in pelagic habitats. We note that all 12 shark species examined are known to frequent demersal habitats (Compagno et al., 2005; Froese and Pauley, 2013). The cestode faunas of the 2 shark species in common between our study and that of Palm and Schröder's (2001) from the Great Meteor Bank differ in a few respects. In the 2 specimens of D. calcea they examined, the latter authors reported post-larvae of Tentacularia coryphaenae Bosc, 1802 and adults of Deanicola minor, whereas, we found adults of D. minor and a second potentially new species of Deanicola, as well as plerocercoids of at least 2 phyllobothriid tetraphyllideans. The absence of T. coryphaenae from our samples is likely the result of differences in organs necropsied; whereas we examined only the spiral intestine, Palm and Schröder (2001) examined all organs. Given the generally low prevalence of cestode infections in deeper water sharks, our larger sample size (13 vs. 2 sharks) may account for the greater diversity reported here from this host species. With respect to Deania profundorum, while we found the cestode fauna to consist solely of a single juvenile specimen of Aporhynchus, Palm and Schröder (2001) reported 5 trypanorhynch species: 3 species as larvae (Tentacularia coryphaenae and 2 Grillotia spp.) and adults of 2 Deanicola species. In this instance, sample sizes were approximately equal (2 vs. 1 shark, respectively). It is possible that a larger sample size would reveal additional adult cestode diversity, given that each of the 3 host specimens examined had a unique fauna of adult tapeworms. However, the existence of a second species resembling D. profundorum (i.e., D. cf. profundorum) occurring sympatrically in the vicinity of the Azores was not revealed until 2012 (see Naylor et al., 2012b) and thus the identities of the hosts of the species reported by Palm and Schröder (2001) require verification in this context. A number of the shark species examined here have been reported to host spiral intestine cestodes in other geographic regions, and even ocean basins, of the world (e.g., Beveridge, 1990; Klimpel et al., 2001). But, as revealed by Naylor et al. (2012b), the identification of host species, especially deep-water sharks that are morphologically similar, can be difficult and thus caution should be exercised when making comparisons without verified and/or vouchered host material. To our knowledge, this is the first report of cestodes from Centroscyllium fabricii and Centroscymnus crepidater, however, due to the low intensity of infection (only a single worm was found in each host species) and the immature condition of both worms, a formal description of the worm is impossible at this time. The identity of the tetraphyllidean plerocercoids found here in D. calcea and Centroscymnus crepidater is intriguing. All appear to represent larval type XV of Jensen and Bullard (2010). Although merocercoids with this scolex form have commonly been referred to in the literature under the names Phyllobothrium delphini (Bosc,
1802) van Beneden, 1868 and/or Monorygma grimaldii (Moniez, 1889) Daly, 1919 (e.g., Augusti et al., 2005a; Siquier and Le Bas, 2003; Testa and Dailey, 1977), molecular data (e.g., Augusti et al., 2005b; Aznar et al., 2007; Jensen and Bullard, 2010) suggest that merocercoids and plerocercoids of this form from cetaceans, and plerocercoids from squid (Brickle et al., 2001) may represent species of Clistobothrium. Unfortunately, plerocercoids from sharks have yet to be included in molecular analyses and thus their affinities to those from these other host species are unclear. Based on scolex morphology our larvae most closely resemble phyllobothriids of the genus Clistobothrium, possibly of 2 species. Among the 4 larval types for which scolex SEM data were presented by Augusti et al. (2005a), our larvae are most similar to the merocercoids they identified as Phyllobothrium delphini. However they differ in their possession of trullate or gladiate spinitriches, rather than “crowned cylindrical spinitriches” (Augusti et al., 2005a, p. 182) on the distal bothrial surfaces. Fortunately, a subset of the worms collected in this study was preserved in ethanol, and thus, future molecular analysis is possible, helping elucidate the relationships and identifications of these larval forms. In total, 57% of the 112 animals necropsied in this study were found to be uninfected. Our results suggest that the cestode faunas of squaliform sharks are indeed depauperate relative to those of most other elasmobranch taxa, a concept supported by some previous literature (e.g., see Host–Parasite list in Palm, 2004). For example, based on data from Beveridge and Justine (2006) and data extracted from the extensive host–parasite list of Palm (2004) both the range of adult trypanorhynch species and average number of trypanorhynch species per squaliform shark species (0–7 and 1.6, respectively for 24 squaliform shark species) are conspicuously lower than those seen in both carcharhiniform (1–18 and 4.1, respectively for 58 carcharhiniform species) and lamniform (1–10 and 4.1, respectively for 9 lamniform species) sharks. Our results for squaliform sharks show a similar pattern. A total of only 12–14 species of cestodes was found across the 12 squaliform shark species examined. On average each shark hosted only 1.75 cestodes of all life cycle stages and 1.2 adult cestodes per shark species. Whether this is a phylogenetic effect, or can be attributed to the fact that essentially all shark species examined here occupy the deeper water habitats remains to be addressed. Nonetheless, our results are consistent with the findings of others investigating parasite faunas of deeper water elasmobranchs (e.g., Campbell, 1983; Palm and Schröder, 2001) in that the faunas were dominated by trypanorhynchs of the families Aporhynchidae and Gilquiniidae and larval tetraphyllideans. Finally, regarding the discrepancies of the identities of 2 species of sharks across our recent publications. For the sake of consistency among papers in this volume we have used Centroscymnus cryptacanthus and Centrosymnus crepidater here despite the fact
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
J.N. Caira, M. Pickering / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
8
that we followed Last and Stevens 2009 and referred to these same specimens as Centroscymnus owstonii and Centroselachus crepidater, respectively in Naylor et al. (2012a, b). Both pairs of species names require further examination because discrepancies exist more widely in the literature. For example, while Eschmeyer (2013) lists Centroscymnus cryptacanthus as a synonym of C. owstonii, C. cryptacanthus is listed as the valid name in the ITIS database (http://www.itis.gov.). In the phylogeny presented by Naylor et al. (2012a), Centroscymnus was recovered as a non-monophyletic genus. This situation was exacerbated by the placement of C. crepidater as sister to the species of Zameus included in the results of their analyses. Adoption of the former species as a member of the monotypic Centroselachus (e.g., Compagno et al., 2005) resolved at least some of this issue. Acknowledgments We are grateful to Dr. Gui Menezes of the Department of Oceanography and Fisheries at the University of Azores for arranging for the collection of sharks by J.N.C. and M.P. during their visits to Horta in 2006 and 2009 and for inviting M.P. to participate in the 2012 Condor Seamount research cruise on the R.V. Arquipélago, as well as for providing laboratory facilities. A big thanks to the scientific staff, especially Eva Giacomello and Diana Catarino, and the crew of the Arquipélago for their aid in the collection of hosts, photographs, recording worm data, and providing accommodations and assistance. This work was supported in part by NSF PBI award nos. 0818823 and 0818696. References Augusti, C., Aznar, F., Raga, J.A., 2005a. Microtriches of tetraphyllidean metacestodes from western Mediterranean striped dolphins (Stenella coeruleoalba). J. Morphol. 265, 1766–1899. Augusti, C., Aznar, F., Olson, P.D., Littlewood, D.T.J., Kostadinova, A., Raga, J.A., 2005b. Morphological and molecular characterization of tetraphyllidean merocercoids (Platyhelminthes: Cestoda) of striped dophins (Stenella coeruleoalba) from the Western Mediterranean. Parasitology 130, 1–14. Aznar, F.J., Agusti, C., Littlewood, D.T.J., Raga, J.A., Olson, P.D., 2007. Insight into the role of cetaceans in the life cycle of the tetraphyllideans (Platyhelminthes: Cestoda). Int. J. Parasitol. 37, 243–255. Beveridge, I., 1990. Revision of the family Gilquiniidae (Cestoda: Trypanorhyncha) from elasmobranch fishes. Aust. J. Zool. 37, 481–520. Beveridge, I., Justine, J.-L., 2006. Gilquiniid cestodes (Trypanorhyncha) from elasmobranch fishes off New Calendonia with descriptions of two new genera and a new species. Syst. Parasitol. 65, 235–249. Brickle, P., Olson, P.D., Littlewood, D.T.J., Bishop, A., Arkhipkin, A.I., 2001. Parasites of Loligo gahi from waters off the Falkland Islands, with a phylogenetic based identification of their cestode larvae. Can. J. Zool. 79, 2289–2296. Campbell, R.A., 1983. Parasitism in the Deep Sea. In Deep-sea Biology, the Sea, vol. 8. Wiley-Interscience, New York, pp. 473–552. Chervy, L., 2002. The terminology of larval cestodes or metacestodes. Syst. Parasitol. 52, 1–33. Chervy, L., 2009. Unified terminology for cestode microtriches: a proposal from the participants of the international workshops on Cestode Systematics in 2002– 2008. Folia Parasitol. 56, 199–230. Compagno, L.J.V., Dando, M., Fowler, S., 2005. Sharks of the World. Collins, London.
Eschmeyer, W.N. (Ed), 2013. Genera, Species, References. 〈http://research.calacademy. org/research/ichthyology/catalog/fishcatmain.asp〉 (electronic version accessed 08.07.13). Euzet, L., 1994. Order Tetraphyllidea Carus, 1863. In Keys to the cestode parasites of vertebrates. Khalil, L. F., A. Jones, and R. A. Bray. CAB International. Wallingford, U. K. 149–194. Froese, R., Pauley, D. (Eds.), 2013. FishBase. World Wide Web Electronic Publication. (〈www.fishbase.org〉 version (04/2013). Giacomello, E., Menezes, G., Bergstad, O. A., An integrated approach for studying seamounts: CONDOR Observatory, this issue. Guiart, J., 1935. Résultats des Campagnes Scientifiques du Albert Ier, Prince Monaco. Cestodes parasites provenant des campagnes scientifiques de S. A. S. le Prince Albert 1er de Monaco (1886–1913). Impr. Monaco, Monaco, 105. Jensen, K., 2005. A monograph on the Lecanicephalidea (Platyhelminthes, Cestoda). Bull. Univ. Nebr. State Mus. 18, 1–241. Jensen, K., Bullard, S.A., 2010. Characterization of diversity of tetraphyllidean and rhinebothriidean cestode larval types, with comments on host associations and life-cycles. Int. J. Parasitol. 40, 889–910. Klimpel, S., Seehagen, A., Palm, H.W., Rosenthal, H., 2001. Deep-Water Metazoan Fish Parasites of the World. Lagos Verlag, Berlin, Germany p. 316. Last, P.R., Stevens, J.D., 2009. Sharks and Rays of Australia, 2nd edition Harvard University Press, Cambridge p. 644. Naylor, G.J.P., Caira, J.N., Jensen, K., Rosana, K.A.M., Straube, N., Lakner, C., 2012a. Elasmobranch phylogeny: a mitochondrial estimate based on 595 species. In: Carrier, J.C., Musick, J.A., Heithaus, M.R. (Eds.), Biology of Sharks and their Relatives. CRC Press, Boca Raton, pp. 31–56. Naylor, G.J.P., Caira, J.N., Jensen, K., Rosana, K.A.M., White, W.T., Last, P.R., 2012b. A DNA sequence-based approach to the identification of shark and ray species and its implications for global elasmobranch diversity and parasitology. Bull. Amer. Mus. Nat. Hist. 367, 1–262. Noever, C., 2009. Diet and Metazoan Parasites of Deep-water Fishes of the Azores (M.Sc. thesis). University Kiel, pp. 1–97. Noever, C., Caira, J.N., Kuchta, R., Desjardins, L., 2010. Two new species of Aporhynchus (Cestoda: Trypanorhyncha) from deep water lantern sharks (Squaliformes: Etmopteridae) in the Azores, Portugal. J. Parasitol. 96, 1176–1184. Obersteiner, W., 1914. Über eine neue Cestodenform Bilocularia hyperapolytica nov. gen. nov. spec., aus Centrophorus granulosus. Arb. Zool. Inst. Univ. Wien Zool. Stn. Trieste 20, 109–124. Olson, P.D., Caira, J.N., Jensen, K., Overstreet, R.M., Palm, H., Beveridge, I., 2010. Evolution of the trypanorhynch tapeworms: parasite phylogeny supports independent lineages of sharks and rays. Int. J. Parasitol. 40, 223–242. Palm, H.W., 2004. The Trypanorhyncha Diesing, 1863. PKSPL IPB Press, Bogor, p. 710. Palm, H.W., Schröder, P., 2001. Cestode parasites from the elasmobranchs Heptrachias perlo and Deania from the Great Meteor Bank, central East Atlantic. Aquat. Living Resour. 14, 137–144. Pickering, M., Caira, J.N., 2008. Calliobothrium schneiderae n. sp. (Cestoda: Tetraphyllidea) from the Spotted Estuary Smooth-hound shark, Mustelus lenticulatus, from New Zealand. Comp. Parasitol. 75, 174–181. Rodriguez, N., Pickering, M., Caira, J.N., 2011. Echinobothrium joshuai n. sp. (Cestoda: Diphyllidea) from the Roughnose Legskate, Cruriraja hulleyi (Rajiformes: Rajidae), off South Africa. Comp. Parasitol. 78, 306–311. Ruhnke, T.R., 2011. A monograph on the Phyllobothriidae (Platyhelminthes: Cestoda). Bull. Univ. Nebr. State Mus. 25, 1–208. Schröder, P., 1999. Parasiten von Fischen der Groben Meteorbank (zentraler Ost-Atlantik) (M.Sc. thesis). University Kiel, pp. 1–69. Siquier, G., Le Bas, A., 2003. Morphometrical categorization of Phyllobothrium delphini (Cestoidea, Tetraphyllidea) cysts from Fraser's dophin, Lagenodelphis hosei (Cetacea, Delphinidae). Lat. Amer. J. Aquat. Mamm. 2, 95–100. Testa, J., Dailey, M.D., 1977. Five new morphotypes of Phyllobothrium delphini (Cestoda: Tetraphyllidea), their relationshiop to existing morphotypes, and their zoogeography. Bull. South Calif. Acad. Sci. 76, 99–110. Tyler, G.A., 2006. A monograph on the Diphyllidea (Platyhelminthes, Cestoda). Tapeworms of Elasmobranchs. Part II. Bull. Univ. Nebr. State Mus. 20, 1–142. Williams, H.H., 1958. Some Phyllobothriidae (Cestoda: Tetraphyllidea) of elasmobranchs from the western seaboard of the British Isles. J. Nat. Hist. Ser. 13 1 (2), 113–136.
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
Contents lists available at ScienceDirect
Deep-Sea Research II journal homepage: www.elsevier.com/locate/dsr2
Cestodes from deep-water squaliform sharks in the Azores Janine N. Caira, Maria Pickering n Department of Ecology & Evolutionary Biology, 75 N. Eagleville Road, Unit 3043, University of Connecticut, Storrs, CT 06269-3043, USA
art ic l e i nf o
Keywords: Azores Cestodes Condor seamount Deep-water sharks Tapeworms
a b s t r a c t The majority of our knowledge on marine tapeworms (cestodes) is limited to taxa that are relatively easy to obtain (i.e., those that parasitize shallower-water species). The invitation to participate in a deepwater research survey off the Condor seamount in the Azores offered the opportunity to gain information regarding parasites of the less often studied sharks of the mesopelagic and bathypelagic zone. All tapeworms (Platyhelminthes: Cestoda) found parasitizing the spiral intestine of squaliform shark species (Elasmobranchii: Squaliformes) encountered as part of this survey, as well as some additional Azorean sampling from previous years obtained from local fishermen are reported. In total, 112 shark specimens of 12 species of squaliform sharks representing 4 different families from depths ranging between 400 and 1290 m were examined. Cestodes were found in the spiral intestines from 11 of the 12 squaliform species examined: Deania calcea, D. cf. profundorum, D. profundorum, Etmopterus princeps, E. pusillus, E. spinax, Centroscyllium fabricii, Centroscymnus coelolepis, C. cryptacanthus, C. crepidater, and Dalatias licha. No cestodes were found in the spiral intestines of Centrophorus squamosus. Light microscopy and scanning electron microscopy revealed several potentially novel trypanorhynch and biloculated tetraphyllidean species. Aporhynchid and gilquiniid trypanorhynchs dominated the adult cestode fauna of Etmopterus and Deania host species, respectively, while larval phyllobothriids were found across several host genera, including, Deania, Centroscyllium, and Centroscymnus. These results corroborate previous findings that deep-water cestode faunas are relatively depauperate and consist primarily of trypanorhynchs of the families Gilquiniidae and Aporhynchidae and larval tetraphyllideans. A subset of specimens of most cestode species was preserved in ethanol for future molecular analysis to allow more definitive determinations of the identification of the larval tetraphyllideans and trypanorhynchs lacking evaginated tentacles and other key diagnostic features. & 2013 Elsevier Ltd. All rights reserved.
1. Introduction Our understanding of the tapeworms that parasitize many of the world's 1200 species of sharks and rays (i.e., elasmobranchs, see Naylor et al., 2012a, 2012b) has expanded considerably over the past two decades (e.g., see Jensen, 2005; Palm, 2004; Ruhnke, 2011; Tyler, 2006). This work has placed particular emphasis on hosts occupying epibenthic and epipelagic habitats (i.e., depths of r200 m) in large part because animals inhabiting these relatively shallow waters are readily accessible and easily procured in collaboration with artisanal fishing enterprises. This is not, however, the case for deeper water elasmobranchs, and sharks in particular. With respect to the two most speciose groups of deepwater sharks (i.e., Squaliformes and Scyliorhinidae), in the most recent comprehensive synopsis of the metazoan parasites of deepwater fishes of the world, Klimpel et al.'s (2001) checklist included
n
Corresponding author. Tel.: þ 1 805 637 6180; fax: þ 1 860 486 6364. E-mail addresses: [email protected] (J.N. Caira), [email protected] (M. Pickering).
cestode (tapeworm) data for only 12 of the 121 species of dogfish sharks (Squaliformes) and only 1 of the 154 species of catsharks (Scyliorhinidae) listed by Compagno et al. (2005). This checklist reveals that the majority of cestodes found parasitizing deepwater hosts consist of larval cestodes in the order Tetraphyllidea and adult cestodes of the order Trypanorhyncha. Although Palm (2004) expanded trypanorhynch cestode records to include 27 species of squaliform hosts and 6 species of scyliorhinid hosts, the tapeworm faunas of the majority of species of deep-water sharks are completely unknown. The Condor seamount project provided an invaluable opportunity for us to expand knowledge of tapeworms of deeper water sharks, and squaliforms in particular. Some of the sharks examined for the purposes of this study had never previously been examined for cestodes; most had never been examined in this region. In fact, to our knowledge, existing data for adult cestodes from deepwater sharks in the vicinity of the Azores come primarily from M.S. (e.g., Schröder, 1999) and Ph.D. (e.g., Noever, 2009) theses, only a subset of the results of which have been formally published (e.g., Palm and Schröder, 2001), in the latter case for the Great
0967-0645/$ - see front matter & 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.dsr2.2013.08.008
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
J.N. Caira, M. Pickering / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
2
Meteor Bank in the central northeast Atlantic, 1000 km south of the Azores. Guiart's (1935) report of cestodes from deep-water sharks in the Azores includes only larvae. Our goal here is to provide preliminary identifications and basic morphological data using scanning electron microscopy and/or light microscopy for the cestode taxa found parasitizing the squaliform shark species examined over the course of the surveys. With the exception of Noever et al. (2010) formal descriptions of the novel tapeworm taxa encountered during this study have yet to be generated and will be published separately, as will the results of analyses conducted on specimens of each tapeworm species preserved for the generation of molecular data. To aid future work we have provided images of most cestode taxa encountered and have deposited representative voucher material in the Lawrence R. Penner Parasitology Collection, University of Connecticut, Storrs, Connecticut, United States. It is our hope that the preliminary morphological identifications provided here can be addressed using molecular data in the near future.
2. Materials and methods Sharks collected in May 2006, January 2009, and October 2012 off Faial Island, Azores resulted in a total of 112 individuals of 12 species of deeper water sharks being examined for cestodes. Specimens in 2006 and 2009 were obtained from local fishermen, which were caught as by-catch on longlines. In 2012 sharks were obtained from longline fish surveys conducted by the University of the Azores on the R.V. Arquipélago in conjunction with the Condor seamount studies (Giacomello et al., this issue), and were collected at depths between 400 m and 1290 m around the Condor seamount between 38141'43″N, 29120'12″W and 38131'24″N, 28159'30″W. Data reported here are for all squaliform taxa examined. With two exceptions host identities and family-level classification follow Naylor et al. (2012a, 2012b). Specimens examined were as follows: Centrophoridae: 4 Centrophorus squamosus, 13 Deania calcea, 1 Deania profundorum, and 1 Deania cf. profundorum (sensu Naylor et al., 2012b); Etmopteridae: 11 Etmopterus princeps, 15 Etmopterus pusillus, 23 Etmopterus spinax, and 6 Centroscyllium fabricii; Somniosidae: 14 Centroscymnus coelolepis, 7 Centroscymnus cryptacanthus (treated as Centroscymnus owstonii by Naylor et al., 2012a, 2012b), and 10 Centroscymnus crepidater (treated as Centroselachus crepidater by Naylor et al., 2012a, 2012b); Dalatiidae: 7 Dalatias licha. Additional details regarding sex, size, and depth of collection for all shark species are provided in Table 1. The specific identity of 30 of the 112 specimens was verified in the molecular analysis of the NADH2 gene
in Naylor et al. (2012b). Voucher tissue samples preserved in 95% ethanol were taken from all 112 specimens; photographs of each shark were also taken. The unique host specimen identification numbers of infected individuals (collection code “AZ” followed by collection number) are provided in relevant sections below, and correspond to those used in Naylor et al. (2012b). Images of most specimens and detailed collection and demographic data of all specimens can be accessed at the following URL: www.elasmobranchs.tapewormdb.uconn.edu by entering the collection code AZ and the appropriate collection number. Data presented are for taxa parasitizing the spiral intestine only. The spiral intestine of each shark was opened with a mid-ventral longitudinal incision, and was examined for cestodes under a stereomicroscope. Cestodes found were preserved in either 95% ethanol for future molecular work or 4% seawater buffered formalin for further morphological examination. The spiral intestines were then fixed in 4% seawater buffered formalin for approximately a week and then transferred to 70% ethanol for long-term storage and further study. Preparations of cestodes as whole mounts and for examination with scanning electron microscopy (SEM) followed standard protocols (e.g., Pickering and Caira, 2008; Rodriguez et al., 2011). Museum abbreviations used are as follows: IPCAS, Institute of Parasitology, Academy of Sciences of the Czech Republic, České Budĕjovice, Czech Republic; LRP, Lawrence R. Penner Parasitology Collection, University of Connecticut, Storrs, Connecticut, United States; MHNFCUP, Museu de História Natural da Faculdade de Ciências da Universidade do Porto, Porto, Portugal; USNPC, United States National Parasite Collection, Beltsville, Maryland, United States. Larval cestode terminology follows Chervy (2002); microthrix terminology follows Chervy (2009). Trypanorhynch classification follows Palm (2004) and Olson et al. (2010).
3. Results In total, 48 (i.e., 43%) of the 112 squaliform sharks examined were found to host cestodes of any life cycle stage (i.e., larva, juvenile, or adult) in their spiral intestine (see Table 1); 35.7% hosted juvenile or adult cestodes. The overall prevalence of infection with cestodes in each species of shark ranged from 0% (Centrophorus squamosus) to 73.9% (Etmopterus spinax). Infections ranged from 1 to 3 cestode species per infected shark. The average number of cestode species (regardless of life cycle stage) found per shark species was 1.75 worm species; excluding larval stages, the average was 1.17. However, as noted below in the
Table 1 Detail of squaliform shark species examined for cestodes and number infected by sex. Shark species
Centrophoridae Centrophorus squamosus Deania calcea Deania cf. profundorum Deania profundorum Dalatiidae Dalatias licha Etmopteridae Centroscyllium fabricii Etmopterus princeps Etmopterus pusillus Etmopterus spinax Somniosidae Centroscymnus coelolepis Centroscymnus owstonii Centroselachus crepidater
Total no. examined
Depth collected (m)
Shark total length (cm)
No. examined (No. infected) females
No. examined (No. infected) males
4 13 1 1
1090–1265 1090–1265 540 451–500
121–129 81–112 95 41
4 (0) 10 (6) 1 (1) 1 (1)
– 3 (0) – –
401–540
114.5–123
–
7 (4)
6 11 15 23
1260–1290 1090–1290 500–850 540–750
57–81.5 48–69.5 24.5–48.5 30–43
5 (1) 7 (0) 7 (2) 22 (16)
1 4 8 1
14 7 10
1090–1290 1090–1265 1051–1265
85–118.5 84.5–114 61–84.5
6 (5) 6 (3) 8 (2)
8 (4) 1 (0) 2 (0)
7
(0) (1) (1) (1)
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
J.N. Caira, M. Pickering / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
detailed data provided for each species, species counts presented are conservative. In several instances it is possible that diversity has been underestimated, and further scrutiny is required to confirm these numbers. A total of 3 to 4 larval cestode species was encountered across the 12 squaliform species examined. In addition, 1–2 juvenile cestode taxa and 12–14 adult cestode species were collected. In the sections that follow, the cestode faunas encountered are treated separately for each of the 12 shark species, which are presented according to shark family group. Unfortunately, definitive identification of many of these cestodes based solely on morphology was hampered by the following: (1) in most cases the number of specimens collected was small, (2) most trypanorhynchs lacked everted tentacles and thus also the diagnostic characteristics required for specific identification, and (3) most tetraphyllideans were either larval or juvenile individuals that lacked the diagnostic proglottid features of these taxa. The adult cestode species that we were able to definitively identify were new to science and have already been formally described (see Noever et al., 2010). We have presented scanning electron micrographs here of as many of the remaining taxa as possible in order to facilitate their future identification.
3.1. Centrophoridae (Gulper Sharks) 3.1.1. Centrophorus squamosus None of the 4 individuals examined was found to host cestodes.
3.1.2. Deania calcea (Infected: AZ-108, AZ-111, AZ-112, AZ-131, AZ-132, AZ-152) Six of the 13 individuals (46.2%) examined hosted cestodes. Five of these hosted specimens of Deanicola Beveridge, 1990. With respect to the 2 known species in this genus, these specimens lack the conspicuous pars post-bulbosa of D. protentus Beveridge, 1990 and we believe they represent 2 distinct species of Deanicola. One (Figs. 1–7; LRP 8063–8085) is generally consistent with D. minor Beveridge, 1990. The second is more robust and at least some specimens exhibit a substantially greater number of testes and we believe potentially represents a new species referred to here as Deanicola sp. 1 (Figs. 8–12; LRP 8086–8107). Given the low number and condition of the specimens we are unable to present prevalence data separately for the 2 forms. SEM reveals that the scoleces of both species bear palmate spinitriches with 13 digits on their proximal surfaces (Figs. 3 and 10), 20 or more digits on the anterior of peduncle (Fig. 5), and 16 digits on the posterior surfaces of the peduncle (Figs. 6 and 11). The spinitriches found on the distal bothrial surfaces are pectinate and bear 5–6 digits (Figs. 4 and 12). The apex of the scolex (Fig. 2) and the distal bothrial surfaces also bear capilliform filitriches; the proximal bothrial surfaces also bear acicular filitriches. Specimens of both forms of Deanicola were preserved in 95% ethanol for future molecular work; the hologenophores of these specimens have been deposited in LRP (8151–8152 for D. minor; 8153 for Deanicola sp. 1). D. calcea also hosted what appear to be two forms of larval tetraphyllidean cestodes. Three sharks hosted plerocercoids (LRP 8108–8113) that bear a close resemblance to Clistobothrium montaukensis Ruhnke, 1993. Two different sizes of this larval stage were found. It is possible that the smaller form (Fig. 21) is merely a younger stage of the larger form (Fig. 22). One shark hosted a plerocercoid (Fig. 23) with a scolex that bears a strong resemblance to the phyllobothriid Clistobothrium carcharodoni Dailey and Vogelbein, 1990.
3
3.1.3. Deania cf. profundorum (Infected: AZ-46) The single specimen of this species examined, which we note based on the results of Naylor et al. (2012b) is not conspecific with Deania profundorum, hosted specimens of a small typanorhynch that appears to belong to the genus Deanicola (LRP 8154–8165). All are immature, but it appears to represent a species different than those seen in D. calcea. 3.1.4. Deania profundorum (Infected: AZ-161) The single specimen of this shark species examined hosted 1 specimen of what appears to be a juvenile of the trypanorhych genus Aporhynchus Nybelin, 1918 (LRP 8148). Its juvenile form makes definitive identification of this specimen impossible at this time. However, it was preserved in 95% ethanol and thus its identity may be confirmed in the future using molecular data. 3.2. Etmopteridae (Lantern Sharks) 3.2.1. Etmopterus princeps (Infected: AZ-104) Only 1 of the 11 individuals (9%) of this species examined was infected. This single shark hosted specimens of 3 species of trypanorhynchs. These include what we believe is a new species of Gilquinia (Figs. 13–18; LRP 8114–8118). Unfortunately, no specimens were found with their tentacles everted. With respect to the 3 known members of this genus, it possesses a greater number of testes than G. stevensi Beveridge, 1990 and fewer testes than G. squali (Fabricius, 1794) Dollfus, 1930 (i.e., 219 vs. 87–108 and 278–348, respectively). The pattern of microtriches on its scolex differs conspicuously from that reported for the third member of the genus, G. robertsoni Beveridge, 1990, by Palm (2004; Figs. 79a–f). SEM shows our specimens to bear acicular filitriches and no spinitriches on the peduncular (Fig. 15) and proximal bothrial (Fig. 16) surfaces, and spathulate spinitriches and capilliform filitriches on its interbothrial (Fig. 17) and distal bothrial (Fig. 18) surfaces. This shark also hosted a single immature specimen of what we believe represents a species of Aporhynchus (LRP 8119). In addition, several specimens that resemble Plesiorhynchus brayi Palm, 2004 reported by Palm (2004), also from the North Atlantic, in overall morphology (Figs. 19 and 20; LRP 8120) were found. 3.2.2. Etmopterus pusillus (Infected: AZ-50, AZ-51, AZ-147) Only 3 of the 15 individuals (20%) of this species examined were infected. These sharks each hosted a few specimens of the new aporhynchid trypanorhynch, Aporhynchus pickeringae Noever, Caira, Kuchta, Desjardins, 2010, the description of which has already been formally communicated (see Noever et al., 2010). The specimens of this species were deposited in museums as follows: Holotype (MHNFCUP no. 078883); scoleces of juveniles of 2 paratypes (USNPC nos. 103217–103218), partial strobilae of 2 paratypes (USNPC nos. 103219–103220); scoleces of juveniles of 2 paratypes (LRP no. 7365), partial strobila of 1 paratype (LRP no. 7364); free proglottid of 1 paratype (IPCAS no. 560). 3.2.3. Etmopterus spinax (Infected: AZ-1, AZ-2, AZ-5, AZ-6, AZ-7, AZ-8, AZ-9, AZ-44, AZ-65, AZ-68, AZ-71, AZ-74, AZ-75, AZ-76, AZ-77, AZ-78, AZ-150) A total of 17 of the 23 specimens (i.e., 73.9%) examined were infected. One shark hosted a single specimen of Aporhynchus norvegicus (USNPC 103221). All 17 sharks hosted juvenile and/or adult specimens of the new aporhynchid trypanorhynch Aporhynchus menezesi Noever, Caira, Kuchta, Desjardins, 2010 the description of which has also already been published (see Noever et al., 2010). The specimens of this species were deposited in museums as follows: Holotype (MHNFCUP no. 078882) and 1 paratype (MHNFCUP no.
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
4
J.N. Caira, M. Pickering / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
Fig. 1–12. Scanning electron micrographs of Deanicola minor and Deanicola sp. 1 cestodes found parasitizing Deania calcea. (1) Scolex of Deanicola minor; scale bar, 100 mm. Note: small numbers correspond to Figs. 2–6, 10–12 showing higher magnification images of these surfaces. (2) Apical surface of scolex in D. minor; scale bar, 2 mm. (3) Proximal surface of scolex in D. minor; scale bar, 2 mm. (4) Distal surface of scolex in D. minor; scale bar, 2 mm. (5) Anterior surface of peduncle in D. minor; scale bar, 100 mm. (6) Posterior surface of peduncle in D. minor; scale bar, 100 mm. (7) Tentacle hooks from D. minor; scale bar, 20 mm. (8) Scolex of Deanicola sp. 1; scale bar, 100 mm. (9) Tentacle hooks from Deanicola sp. 1; scale bar, 20 mm. (10) Proximal surface of scolex in Deanicola sp. 1; scale bar, 2 mm. (11) Peduncle surface of scolex in Deanicola sp. 1; scale bar, 2 mm. (12) Distal surface of scolex in Deanicola sp. 1; scale bar, 2 mm.
078884); 1 paratype (IPCAS no. C–560); 3 paratypes (USNPC no. 103216); 1 paratype (LRP no. 7366), cross sections of terminal proglottid of 1 paratype and its strobilar voucher (LRP nos. 7374–7382), cross sections of scolex of paratype (LRP nos. 7370–7373), 3 paratypes prepared for SEM and their strobilar vouchers (LRP nos. 7367–7369), 2 egg preparations (LRP nos. 7383–7384); 3 juvenile specimens (LRP nos. 7385–7387). In addition, one specimen of a juvenile tetraphyllidean was found and saved in ethanol for future molecular analysis and identification.
3.2.4. Centroscyllium fabricii (Infected: AZ-106) Only one of the 6 individuals (17.7%) of this species was infected and this infection consisted of only a single cestode specimen (LRP 8121). We believe it belongs to the genus Gilquinia,
but given that its tentacles are retracted this identification requires confirmation. 3.3. Somniosidae (Sleeper Sharks) 3.3.1. Centroscymnus coelolepis (Infected: AZ-84, AZ-85, AZ-86, AZ-87, AZ-114, AZ-115, AZ-125, AZ-126, AZ-133) Nine of the 14 specimens (i.e., 64.3%) of this species examined hosted cestodes. All 9 hosted immature or adult specimens of a phyllobothriid tetraphyllidean bearing biloculated bothridia. Despite the fact that a number of these specimens are fully mature, we are unable to confidently place them in a known genus at this time. Among the phyllobothriid genera considered valid by Ruhnke (2011), they most closely resemble Monorygma Diesing, 1863 but lack the posterior lateral projections on the
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
J.N. Caira, M. Pickering / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
5
Fig. 13–20. Scanning electron micrographs of Gilquinia sp. 1 and Plesiorhynchus sp. cestodes found parasitizing Etmopterus princeps. (13) Scolex of Gilquinia sp. 1; scale bar, 500 mm. Small number indicates location of detail shown in Fig. 15. (14) Scolex proper of Gilquinia sp. 1; scale bar, 200 mm. Small number indicates location of detail shown in Figs. 16–18. (15) Peduncle surface of Gilquinia sp. 1; scale bar, 2 mm. (16) Proximal surface of Gilquinia sp. 1; scale bar, 2 mm. (17) Surface between bothria of Gilquinia sp. 1; scale bar, 2 mm. (18) Distal surface of Gilquinia sp. 1; scale bar, 2 mm. (19) Scolex of Plesiorhynchus sp.; scale bar, 500 mm. (20) Scolex proper of Plesiorhynchus sp.; scale bar, 200 mm.
anterior loculus seen in members of this genus. Both a smaller (Fig. 25; LRP 8122–8127) and larger (Fig. 27; LRP 8128–8135) form of this taxon was encountered and it is possible they represent different species. The bothridia of the scoleces of both forms were covered with small gladiate spinitriches on all surfaces (Fig. 26). Specimens of both forms were preserved in 95% ethanol for future molecular work. Until these taxonomic issues can be resolved we have combined data for both forms. One shark also hosted specimens of plerocercoids (LRP 8149–8150) resembling Clistobothrium montaukensis like those seen in Deania calcea.
hosted plerocercoids resembling those of C. montaukensis like those seen in D. calcea (LRP 8136). One shark hosted a merocercoid (LRP 8137) like that seen in C. coelolepis. 3.3.3. Centroscymnus crepidater (¼Centroselachus crepidater of Naylor et al., 2012a, 2012b) (Infected: AZ-122, AZ-144) Only 2 of the 10 individuals (i.e., 20%) of this species examined were infected. Both (Fig. 24; LRP 8138) hosted plerocercoids resembling C. montaukensis like those seen in D. calcea. 3.4. Dalatiidae (Kitefin Sharks)
3.3.2. Centroscymnus cryptacanthus ( ¼Centroscymnus owstonii of Naylor et al. 2012a, 2012b) (Infected: AZ-129, AZ-142, AZ-143) Three of the 7 individuals (i.e., 42.9%) of this species examined were infected, but in all cases only with larval forms. Two sharks
3.4.1. Dalatias licha (Infected: AZ-3, AZ-79, AZ-160, AZ-163) Four of the 7 individuals (i.e., 57.1%) examined were found to host cestodes. All 4 hosted numerous mature and gravid proglottids
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
6
J.N. Caira, M. Pickering / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
Fig. 21–27. Scanning electron micrographs of larval tetraphyllidean cestodes found in spiral intestines of squaliform sharks. (21) Smaller form resembling Clistobothrium montaukensis from Deania calcea; scale bar, 200 mm. (22) Larger form resembling Clistobothrium montaukensis from Deania calcea; scale bar, 500 mm. (23) Specimen resembling Clistobothrium carcharodon from Deania calcea; scale bar, 200 mm. (24) Specimen resembling Clistobothrium montaukensis from Centroscymnus crepidater; scale bar, 500 mm. (25) Scolex of smaller form of unidentified biloculate tetraphyllidean genus from Centroscymnus coelolepis; scale bar, 200 mm. Small number indicates location of detail shown in Fig. 26. (26) Distal surface of unidentified biloculate tetraphyllidean genus from Centroscymnus coelolepis; scale bar, 1 mm. (27) Scolex of larger form of unidentified biloculate tetraphyllidean genus from Centroscymnus coelolepis; scale bar, 500 mm.
(LRP 8139–8146) that are easily identified as Bilocularia hyperapolytica Obersteiner, 1914. One shark also hosted a small juvenile worm with no proglottids (LRP 8147) but bearing a scolex with 4 biloculated bothridia. This worm resembles the hyperapolytic form of B. hyperapolytica reported and illustrated by Obersteiner (1914). Euzet (1994) considered Bilocularia Obersteiner, 1914 to be a genus inquirendum as it had not been reported from its type host “Centrophorus granuluosus” since its original description. However, Williams (1958) reported finding numerous proglottids of this species in the single specimen of D. licha (as Scymnus licha) he examined off the British Isles. Williams found no scoleces, but noted that the proglottids were strikingly similar to those illustrated by Obersteiner (1914). Our results confirm D. licha as an appropriate host for this species and lead us to speculate that the identity of the type host may have been in error.
4. Discussion Infection data for the 12 species of deep-water sharks examined here are summarized in Fig. 28 by ocean zone of capture. However, it should be noted that all 12 species are known to occur in both meso- and bathyal zones (Compagno et al., 2005; Froese and Pauley, 2013). Regardless of sample size, with the exception of C. squamosus, one or more species of cestode was found parasitizing the spiral intestine of all shark species collected. Previous work on parasites of deeper water sharks (e.g., Campbell, 1983) leads us to believe that within ocean zones these infections are more likely to have occurred in benthic rather than in pelagic situations. This is because the complex life-cycles of cestodes rely on trophic transmission among hosts and the number and diversity of potential intermediate hosts is generally greater in benthic, or at
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
J.N. Caira, M. Pickering / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
7
Fig. 28. Summary of spiral intestine cestode data by ocean zone of capture for the 12 deep-water shark species examined here. Shark families are indicated as follows: (C) Centrophoridae; (D) Dalatiidae; (E) Etmopteridae; (S) Somniosidae.
least demersal, habitats than in pelagic habitats. We note that all 12 shark species examined are known to frequent demersal habitats (Compagno et al., 2005; Froese and Pauley, 2013). The cestode faunas of the 2 shark species in common between our study and that of Palm and Schröder's (2001) from the Great Meteor Bank differ in a few respects. In the 2 specimens of D. calcea they examined, the latter authors reported post-larvae of Tentacularia coryphaenae Bosc, 1802 and adults of Deanicola minor, whereas, we found adults of D. minor and a second potentially new species of Deanicola, as well as plerocercoids of at least 2 phyllobothriid tetraphyllideans. The absence of T. coryphaenae from our samples is likely the result of differences in organs necropsied; whereas we examined only the spiral intestine, Palm and Schröder (2001) examined all organs. Given the generally low prevalence of cestode infections in deeper water sharks, our larger sample size (13 vs. 2 sharks) may account for the greater diversity reported here from this host species. With respect to Deania profundorum, while we found the cestode fauna to consist solely of a single juvenile specimen of Aporhynchus, Palm and Schröder (2001) reported 5 trypanorhynch species: 3 species as larvae (Tentacularia coryphaenae and 2 Grillotia spp.) and adults of 2 Deanicola species. In this instance, sample sizes were approximately equal (2 vs. 1 shark, respectively). It is possible that a larger sample size would reveal additional adult cestode diversity, given that each of the 3 host specimens examined had a unique fauna of adult tapeworms. However, the existence of a second species resembling D. profundorum (i.e., D. cf. profundorum) occurring sympatrically in the vicinity of the Azores was not revealed until 2012 (see Naylor et al., 2012b) and thus the identities of the hosts of the species reported by Palm and Schröder (2001) require verification in this context. A number of the shark species examined here have been reported to host spiral intestine cestodes in other geographic regions, and even ocean basins, of the world (e.g., Beveridge, 1990; Klimpel et al., 2001). But, as revealed by Naylor et al. (2012b), the identification of host species, especially deep-water sharks that are morphologically similar, can be difficult and thus caution should be exercised when making comparisons without verified and/or vouchered host material. To our knowledge, this is the first report of cestodes from Centroscyllium fabricii and Centroscymnus crepidater, however, due to the low intensity of infection (only a single worm was found in each host species) and the immature condition of both worms, a formal description of the worm is impossible at this time. The identity of the tetraphyllidean plerocercoids found here in D. calcea and Centroscymnus crepidater is intriguing. All appear to represent larval type XV of Jensen and Bullard (2010). Although merocercoids with this scolex form have commonly been referred to in the literature under the names Phyllobothrium delphini (Bosc,
1802) van Beneden, 1868 and/or Monorygma grimaldii (Moniez, 1889) Daly, 1919 (e.g., Augusti et al., 2005a; Siquier and Le Bas, 2003; Testa and Dailey, 1977), molecular data (e.g., Augusti et al., 2005b; Aznar et al., 2007; Jensen and Bullard, 2010) suggest that merocercoids and plerocercoids of this form from cetaceans, and plerocercoids from squid (Brickle et al., 2001) may represent species of Clistobothrium. Unfortunately, plerocercoids from sharks have yet to be included in molecular analyses and thus their affinities to those from these other host species are unclear. Based on scolex morphology our larvae most closely resemble phyllobothriids of the genus Clistobothrium, possibly of 2 species. Among the 4 larval types for which scolex SEM data were presented by Augusti et al. (2005a), our larvae are most similar to the merocercoids they identified as Phyllobothrium delphini. However they differ in their possession of trullate or gladiate spinitriches, rather than “crowned cylindrical spinitriches” (Augusti et al., 2005a, p. 182) on the distal bothrial surfaces. Fortunately, a subset of the worms collected in this study was preserved in ethanol, and thus, future molecular analysis is possible, helping elucidate the relationships and identifications of these larval forms. In total, 57% of the 112 animals necropsied in this study were found to be uninfected. Our results suggest that the cestode faunas of squaliform sharks are indeed depauperate relative to those of most other elasmobranch taxa, a concept supported by some previous literature (e.g., see Host–Parasite list in Palm, 2004). For example, based on data from Beveridge and Justine (2006) and data extracted from the extensive host–parasite list of Palm (2004) both the range of adult trypanorhynch species and average number of trypanorhynch species per squaliform shark species (0–7 and 1.6, respectively for 24 squaliform shark species) are conspicuously lower than those seen in both carcharhiniform (1–18 and 4.1, respectively for 58 carcharhiniform species) and lamniform (1–10 and 4.1, respectively for 9 lamniform species) sharks. Our results for squaliform sharks show a similar pattern. A total of only 12–14 species of cestodes was found across the 12 squaliform shark species examined. On average each shark hosted only 1.75 cestodes of all life cycle stages and 1.2 adult cestodes per shark species. Whether this is a phylogenetic effect, or can be attributed to the fact that essentially all shark species examined here occupy the deeper water habitats remains to be addressed. Nonetheless, our results are consistent with the findings of others investigating parasite faunas of deeper water elasmobranchs (e.g., Campbell, 1983; Palm and Schröder, 2001) in that the faunas were dominated by trypanorhynchs of the families Aporhynchidae and Gilquiniidae and larval tetraphyllideans. Finally, regarding the discrepancies of the identities of 2 species of sharks across our recent publications. For the sake of consistency among papers in this volume we have used Centroscymnus cryptacanthus and Centrosymnus crepidater here despite the fact
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i
J.N. Caira, M. Pickering / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎
8
that we followed Last and Stevens 2009 and referred to these same specimens as Centroscymnus owstonii and Centroselachus crepidater, respectively in Naylor et al. (2012a, b). Both pairs of species names require further examination because discrepancies exist more widely in the literature. For example, while Eschmeyer (2013) lists Centroscymnus cryptacanthus as a synonym of C. owstonii, C. cryptacanthus is listed as the valid name in the ITIS database (http://www.itis.gov.). In the phylogeny presented by Naylor et al. (2012a), Centroscymnus was recovered as a non-monophyletic genus. This situation was exacerbated by the placement of C. crepidater as sister to the species of Zameus included in the results of their analyses. Adoption of the former species as a member of the monotypic Centroselachus (e.g., Compagno et al., 2005) resolved at least some of this issue. Acknowledgments We are grateful to Dr. Gui Menezes of the Department of Oceanography and Fisheries at the University of Azores for arranging for the collection of sharks by J.N.C. and M.P. during their visits to Horta in 2006 and 2009 and for inviting M.P. to participate in the 2012 Condor Seamount research cruise on the R.V. Arquipélago, as well as for providing laboratory facilities. A big thanks to the scientific staff, especially Eva Giacomello and Diana Catarino, and the crew of the Arquipélago for their aid in the collection of hosts, photographs, recording worm data, and providing accommodations and assistance. This work was supported in part by NSF PBI award nos. 0818823 and 0818696. References Augusti, C., Aznar, F., Raga, J.A., 2005a. Microtriches of tetraphyllidean metacestodes from western Mediterranean striped dolphins (Stenella coeruleoalba). J. Morphol. 265, 1766–1899. Augusti, C., Aznar, F., Olson, P.D., Littlewood, D.T.J., Kostadinova, A., Raga, J.A., 2005b. Morphological and molecular characterization of tetraphyllidean merocercoids (Platyhelminthes: Cestoda) of striped dophins (Stenella coeruleoalba) from the Western Mediterranean. Parasitology 130, 1–14. Aznar, F.J., Agusti, C., Littlewood, D.T.J., Raga, J.A., Olson, P.D., 2007. Insight into the role of cetaceans in the life cycle of the tetraphyllideans (Platyhelminthes: Cestoda). Int. J. Parasitol. 37, 243–255. Beveridge, I., 1990. Revision of the family Gilquiniidae (Cestoda: Trypanorhyncha) from elasmobranch fishes. Aust. J. Zool. 37, 481–520. Beveridge, I., Justine, J.-L., 2006. Gilquiniid cestodes (Trypanorhyncha) from elasmobranch fishes off New Calendonia with descriptions of two new genera and a new species. Syst. Parasitol. 65, 235–249. Brickle, P., Olson, P.D., Littlewood, D.T.J., Bishop, A., Arkhipkin, A.I., 2001. Parasites of Loligo gahi from waters off the Falkland Islands, with a phylogenetic based identification of their cestode larvae. Can. J. Zool. 79, 2289–2296. Campbell, R.A., 1983. Parasitism in the Deep Sea. In Deep-sea Biology, the Sea, vol. 8. Wiley-Interscience, New York, pp. 473–552. Chervy, L., 2002. The terminology of larval cestodes or metacestodes. Syst. Parasitol. 52, 1–33. Chervy, L., 2009. Unified terminology for cestode microtriches: a proposal from the participants of the international workshops on Cestode Systematics in 2002– 2008. Folia Parasitol. 56, 199–230. Compagno, L.J.V., Dando, M., Fowler, S., 2005. Sharks of the World. Collins, London.
Eschmeyer, W.N. (Ed), 2013. Genera, Species, References. 〈http://research.calacademy. org/research/ichthyology/catalog/fishcatmain.asp〉 (electronic version accessed 08.07.13). Euzet, L., 1994. Order Tetraphyllidea Carus, 1863. In Keys to the cestode parasites of vertebrates. Khalil, L. F., A. Jones, and R. A. Bray. CAB International. Wallingford, U. K. 149–194. Froese, R., Pauley, D. (Eds.), 2013. FishBase. World Wide Web Electronic Publication. (〈www.fishbase.org〉 version (04/2013). Giacomello, E., Menezes, G., Bergstad, O. A., An integrated approach for studying seamounts: CONDOR Observatory, this issue. Guiart, J., 1935. Résultats des Campagnes Scientifiques du Albert Ier, Prince Monaco. Cestodes parasites provenant des campagnes scientifiques de S. A. S. le Prince Albert 1er de Monaco (1886–1913). Impr. Monaco, Monaco, 105. Jensen, K., 2005. A monograph on the Lecanicephalidea (Platyhelminthes, Cestoda). Bull. Univ. Nebr. State Mus. 18, 1–241. Jensen, K., Bullard, S.A., 2010. Characterization of diversity of tetraphyllidean and rhinebothriidean cestode larval types, with comments on host associations and life-cycles. Int. J. Parasitol. 40, 889–910. Klimpel, S., Seehagen, A., Palm, H.W., Rosenthal, H., 2001. Deep-Water Metazoan Fish Parasites of the World. Lagos Verlag, Berlin, Germany p. 316. Last, P.R., Stevens, J.D., 2009. Sharks and Rays of Australia, 2nd edition Harvard University Press, Cambridge p. 644. Naylor, G.J.P., Caira, J.N., Jensen, K., Rosana, K.A.M., Straube, N., Lakner, C., 2012a. Elasmobranch phylogeny: a mitochondrial estimate based on 595 species. In: Carrier, J.C., Musick, J.A., Heithaus, M.R. (Eds.), Biology of Sharks and their Relatives. CRC Press, Boca Raton, pp. 31–56. Naylor, G.J.P., Caira, J.N., Jensen, K., Rosana, K.A.M., White, W.T., Last, P.R., 2012b. A DNA sequence-based approach to the identification of shark and ray species and its implications for global elasmobranch diversity and parasitology. Bull. Amer. Mus. Nat. Hist. 367, 1–262. Noever, C., 2009. Diet and Metazoan Parasites of Deep-water Fishes of the Azores (M.Sc. thesis). University Kiel, pp. 1–97. Noever, C., Caira, J.N., Kuchta, R., Desjardins, L., 2010. Two new species of Aporhynchus (Cestoda: Trypanorhyncha) from deep water lantern sharks (Squaliformes: Etmopteridae) in the Azores, Portugal. J. Parasitol. 96, 1176–1184. Obersteiner, W., 1914. Über eine neue Cestodenform Bilocularia hyperapolytica nov. gen. nov. spec., aus Centrophorus granulosus. Arb. Zool. Inst. Univ. Wien Zool. Stn. Trieste 20, 109–124. Olson, P.D., Caira, J.N., Jensen, K., Overstreet, R.M., Palm, H., Beveridge, I., 2010. Evolution of the trypanorhynch tapeworms: parasite phylogeny supports independent lineages of sharks and rays. Int. J. Parasitol. 40, 223–242. Palm, H.W., 2004. The Trypanorhyncha Diesing, 1863. PKSPL IPB Press, Bogor, p. 710. Palm, H.W., Schröder, P., 2001. Cestode parasites from the elasmobranchs Heptrachias perlo and Deania from the Great Meteor Bank, central East Atlantic. Aquat. Living Resour. 14, 137–144. Pickering, M., Caira, J.N., 2008. Calliobothrium schneiderae n. sp. (Cestoda: Tetraphyllidea) from the Spotted Estuary Smooth-hound shark, Mustelus lenticulatus, from New Zealand. Comp. Parasitol. 75, 174–181. Rodriguez, N., Pickering, M., Caira, J.N., 2011. Echinobothrium joshuai n. sp. (Cestoda: Diphyllidea) from the Roughnose Legskate, Cruriraja hulleyi (Rajiformes: Rajidae), off South Africa. Comp. Parasitol. 78, 306–311. Ruhnke, T.R., 2011. A monograph on the Phyllobothriidae (Platyhelminthes: Cestoda). Bull. Univ. Nebr. State Mus. 25, 1–208. Schröder, P., 1999. Parasiten von Fischen der Groben Meteorbank (zentraler Ost-Atlantik) (M.Sc. thesis). University Kiel, pp. 1–69. Siquier, G., Le Bas, A., 2003. Morphometrical categorization of Phyllobothrium delphini (Cestoidea, Tetraphyllidea) cysts from Fraser's dophin, Lagenodelphis hosei (Cetacea, Delphinidae). Lat. Amer. J. Aquat. Mamm. 2, 95–100. Testa, J., Dailey, M.D., 1977. Five new morphotypes of Phyllobothrium delphini (Cestoda: Tetraphyllidea), their relationshiop to existing morphotypes, and their zoogeography. Bull. South Calif. Acad. Sci. 76, 99–110. Tyler, G.A., 2006. A monograph on the Diphyllidea (Platyhelminthes, Cestoda). Tapeworms of Elasmobranchs. Part II. Bull. Univ. Nebr. State Mus. 20, 1–142. Williams, H.H., 1958. Some Phyllobothriidae (Cestoda: Tetraphyllidea) of elasmobranchs from the western seaboard of the British Isles. J. Nat. Hist. Ser. 13 1 (2), 113–136.
Please cite this article as: Caira, J.N., Pickering, M., Cestodes from deep-water squaliform sharks in the Azores. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2013.08.008i