Advertisement

Revealing trophic transmission pathways of marine tapeworms

  • Jerusha BennettEmail author
  • Fátima Jorge
  • Robert Poulin
  • Haseeb Randhawa
Genetics, Evolution, and Phylogeny - Original Paper
  • 42 Downloads

Abstract

Parasites are important components of natural systems, and among their various roles, parasites strongly influence the flow of energy between and within food webs. Over 1000 tapeworm species are known to parasitise elasmobranchs, although full life cycles are resolved for fewer than 10 of them. The lack in resolution stems from the inability to distinguish larval from adult stages using morphology alone. Molecular elucidation of trophic transmission pathways is the next step in understanding the role of hosts and parasites within food webs. We investigated the parasite assemblage of New Zealand’s rough skate, Zearaja nasuta. Skates and their prey items (obtained from the skates’ stomachs) were dissected for the recovery of adult and larval tapeworms, respectively. A fragment of the 28S rDNA region was amplified for worm specimens with the aim to confirm species identity of parasites within rough skates and to uncover trophic transmission pathways that exploit the predation links between rough skates and their prey. We identified seven species of tapeworms from four tapeworm orders. Four trophic transmission pathways were resolved between three prey items from skates stomachs and skates, and one pathway between larval tapeworm sequence from a New Zealand sole and skate, i.e. a genetic match was found between larval tapeworms in prey and adult worms in skates. We report the first case of an adult trypanorhynch parasitising rough skate. These findings contribute to our limited understanding of cestode life cycles as well as providing insights into the importance of predator-prey relationships for parasite transmission.

Keywords

Trophic transmission Tapeworm Zearaja nasuta 28s rDNA Acanthobothrium Echeneibothrium 

Notes

Acknowledgements

The authors are grateful to Gavin Heineman (Captain of the Echo F/V) for collecting the skate specimens and to Olwyn Friesen, Brandon Ruehle and Bronwen Presswell for help with the skate dissections.

Funding information

This work was financially supported by the Zoology Department and Ecology Degree Programme student budgets, University of Otago.

Compliance with ethical standards

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution at which the studies were conducted.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

436_2019_6264_MOESM1_ESM.docx (34 kb)
ESM 1 (DOCX 34 kb)
436_2019_6264_MOESM2_ESM.pdf (2.7 mb)
ESM 2 Bayesian 50% majority-rule inference for the partial 28S rDNA dataset. (PDF 2718 kb)

References

  1. Abe N, Maehara T, Kashino M, Ohyama M (2011) Identification of parasites found in fresh fish by morphological and sequencing analyses. Annual Report of Osaka City Institute of Public Health and Environmental Sciences 73:2937Google Scholar
  2. Agusti C, Aznar FJ, Olson PD, Littlewood DTJ, Kostadinova A, Raga JA (2005) Morphological and molecular characterization of tetraphyllidean merocercoids (Platyhelminthes: Cestoda) of striped dolphins (Stenella coeruleoalba) from the Western Mediterranean. Parasitology 130:461–474CrossRefPubMedGoogle Scholar
  3. Albert et al (1999) Inkscape.v.0.9 http://www.inkscape.org/
  4. Alexander CG (1963) Tetraphyllidean and diphyllidean cestodes of New Zealand selachians. Transactions of the Royal Society of New Zealand 3:117–142Google Scholar
  5. Alves P, de Chambrier A, Scholz T, Luque J (2015) A new genus and species of proteocephalidean tapeworm (Cestoda), first parasite found in the driftwood catfish Tocantinsia piresi (Siluriformes: Auchenipteridae) from Brazil. Folia Parasitol 62:006CrossRefGoogle Scholar
  6. Amundsen PA, Lafferty KD, Knudsen R, Primicerio R, Klemetsen A, Kuris AM (2009) Food web topology and parasites in the pelagic zone of a subantarctic lake. J Anim Ecol 78:563–572CrossRefPubMedGoogle Scholar
  7. Anglade T, Randhawa HS (2018) Gaining insights into the ecological role of the New Zealand sole (Peltorhamphus novaezeelandiae) through parasites. J Helminthol 92:187–196CrossRefPubMedGoogle Scholar
  8. Arredondo NJ, Alves PV, Gil de Pertierra AA (2017) A new genus of proteocephalid tapeworm (Cestoda) from the marled swamp eel Synbrachus marmoratus Bloch (Synbranchiformes: Synbranchidae) in the river Parana basin, Argentina. Folia Parasitol 64:015CrossRefGoogle Scholar
  9. Ash A, Scholz T, de Chambrier A, Brabec J, Oros M, Kar PK, Chavan SP, Mariaux J (2012) Revision of Gangesia (Cestoda: Proteocephalidea) in the indomalayan region: morphology, molecules and surface ultrastructure. PLoS One 7:E46421CrossRefPubMedPubMedCentralGoogle Scholar
  10. Aznar FJ, Agustí C, Littlewood DTJ, Raga JA, Olson PD (2007) Insight into the role of cetaceans in the life cycle of the tetraphyllideans (Platyhelminthes: Cestoda). Int J Parasitol 37:234–255CrossRefGoogle Scholar
  11. Baum JK, Worm B (2009) Cascading top-down effects of changing oceanic predator abundances. J Anim Ecol 78:699–714CrossRefPubMedGoogle Scholar
  12. Beer A, Ingram T, Randhawa HS (in press) Role of ecology and phylogeny in determining tapeworm assemblages in skates (Rajiformes). J Helmintholi:1–14.  https://doi.org/10.1017/S0022149X18000809
  13. Benesh DP (2010) What are the evolutionary constraints on larval growth in a trophically transmitted parasite? Oecologia 162:599–608CrossRefPubMedGoogle Scholar
  14. Benesh DP, Chubb JC, Parker GA (2014) The trophic vacuum and the evolution of complex life cycles in trophically transmitted helminths. Proc R Soc B 281:20141462CrossRefPubMedGoogle Scholar
  15. Bennett J, Randhawa HS (2019) Diet composition of New Zealand’s endemic rough skate, Zearaja nasuta. New Zeal J Mar Fresh 53(1):162–168CrossRefGoogle Scholar
  16. Blasco-Costa I, Poulin R (2017) Parasite life-cycle studies: a plea to resurrect an old parasitological tradition. J Helminthol 91:647–656CrossRefPubMedGoogle Scholar
  17. Brabec J, Kuchta R, Scholz T (2006) Paraphyly of the Pseudophyllidea (Platyhelminthes: Cestoda): circumscription of monophyletic clades based on phylogenetic analysis of ribosomal RNA. Int J Parasitol 36:1535–1541CrossRefPubMedGoogle Scholar
  18. Brabec J, Waeschenbach A, Scholz T, Littlewood DTJ, Kuchta R (2015) Molecular phylogeny of the Bothriocephalidea (Cestoda): molecular data challenge morphological classification. Int J Parasitol 45(12):761–771CrossRefPubMedGoogle Scholar
  19. Brickle P, Olson PD, Littlewood DTJ, Bishop A, Arkhipkin AI (2001) Parasites of Loligo gahi from waters off the Falkland Islands, with a phylogenetically based identification of their cestode larvae. Can J Zool 79:2289–2296CrossRefGoogle Scholar
  20. Bueno VM (2018) Skate tapeworms revisited: a modern approach. Dissertation, University of ConnecticutGoogle Scholar
  21. Bueno VM, Caira JN (2017) Redescription and molecular assessment of relationships among three species of Echeneibothrium (Rhinebothriidea: Echeneibothriidae) parasitizing yellownose skate, Dipturus chilensis, in Chile. J Parasitol 103:268–284CrossRefPubMedGoogle Scholar
  22. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al., revisited. J Parasitol 83:45–52CrossRefGoogle Scholar
  23. Caira JN (2011) Synergy advances parasite taxonomy and systematics: an example from elasmobranch tapeworms. Parasitology 138:1675–1687CrossRefPubMedGoogle Scholar
  24. Caira JN, Healy CJ (2004) Elasmobranchs as hosts of metazoan parasites. In: Musick JA, Carrier JC, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 523–551CrossRefGoogle Scholar
  25. Caira JN, Jensen K (2014) A digest of elasmobranch tapeworms. J Parasitol 100:373–391CrossRefPubMedGoogle Scholar
  26. Caira JN, Jensen K (eds) (2017) Planetary biodiversity inventory (2008–2017): tapeworms from vertebrate bowels of the earth. Natural History Museum, University of Kansas, LawrenceGoogle Scholar
  27. Caira JN, Reyda F (2005) Marine eucestodes. In: Rohde K (ed) Marine parasitology. CSIRO Press, Canberra, pp 92–104Google Scholar
  28. Caira JN, Jensen K, Holsinger KE (2003) On a new index of host specificity. In: Combes C, Jourdane J (eds) Taxonomie, éecologie et évolution des métazoaires parasites (Livre hommage à Louis Euzet), vol 1. Presse Universitaire de Perpignan, Perpignan, pp 161–201Google Scholar
  29. Caira JN, Marques FPL, Jensen K, Kuchta R, Ivanov V (2013) Phylogenetic analysis and reconfiguration of genera in the cestode order Diphyllidea. Int J Parasitol 43:621–639CrossRefPubMedGoogle Scholar
  30. Caira JN, Jensen K, Waeschenbach A, Olson PD, Littlewood DTJ (2014) Orders out of chaos—molecular phylogenetics reveals the complexity of shark and stingray tapeworm relationships. Int J Parasitol 44:55–73CrossRefPubMedGoogle Scholar
  31. Campbell RA, Beveridge I (1994) Chapter 7: order Trypanorhyncha Diesing, 1863. In: Khalil LF, Jones A, Bray RAI (eds) Keys to the cestode parasites of vertebrates. CABI, Wallingford, pp 51–148Google Scholar
  32. Canard EF, Mouquet N, Mouillot D, Stanko M, Moklisova D, Gravel D (2014) Empirical evaluation of neutral interactions in host-parasite networks. Am Nat 183:468–479CrossRefPubMedGoogle Scholar
  33. Carvajal J, Dailey MD (1975) Three new species of Echeneibothrium (Cestoda: Tetraphyllidea) from the skate, Raja chilensis Guichenot, 1848, with comments on mode of attachment and host specificity. J Parasitol 61:89–94CrossRefPubMedGoogle Scholar
  34. Carvajal J, Goldstein RJ (1971) Acanthobothrium annapinkiensis sp. n. (Cestoda: Tetraphyllidea: Onchobothriidae) from the skate Raja chilensis (Chondrichthyes: Rajiidae) from Chile. Zool Anz 186:158–162Google Scholar
  35. Chambers CB, Cribb TH, Jones MK (2000) Tetraphyllidean metacestodes of teleosts of the great barrier reef, and the use of in vitro cultivation to identify them. Folia Parasitol 47:285–292CrossRefPubMedGoogle Scholar
  36. Chervy L (2002) The terminology of larval cestodes or metacestodes. Syst Parasitol 52:1–33CrossRefGoogle Scholar
  37. Choisy M, Brown SP, Lafferty KD, Thomas F (2003) Evolution of trophic transmission in parasites: why add intermediate hosts? Am Nat 162:172–181CrossRefPubMedGoogle Scholar
  38. Cirtwill AR, Lagrue C, Poulin R, Stouffer DB (2017) Host taxonomy constrains the properties of trophic transmission routes for parasites in lake food webs. Ecology 98:2401–2412CrossRefPubMedGoogle Scholar
  39. Clopper C, Pearson ES (1934) The use of confidence or fiducial limits illustrated in the case of the binomial. Biometri 26:404–413CrossRefGoogle Scholar
  40. Crooks KR, Soulé ME (1999) Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400:563–566CrossRefGoogle Scholar
  41. de Chambrier A, Zehnder M, Vaucher C, Mariaux J (2004) The evolution of the Proteocephalidea (Platyhelminthes, Eucestoda) based on an enlarged molecular phylogeny, with comments on their uterine development. Syst Parasitol 57:159–171CrossRefPubMedGoogle Scholar
  42. de Chambrier A, Waeschenbach A, Fisseha M, Scholz T, Mariaux J (2015) A large 28S rDNA-based phylogeny confirms the limitations of established morphological characters for classification of proteocephalidean tapeworms (Platyhelminthes, Cestoda). Zookeys 500:25–59CrossRefGoogle Scholar
  43. Devlin CM, Diamond AW, Saunders GW (2004) Sexing Arctic terns in the field and laboratory. Waterbirds 27:314–320CrossRefGoogle Scholar
  44. Duffy JE (2002) Biodiversity and ecosystem function: the consumer connection. Oikos 99:201–219CrossRefGoogle Scholar
  45. Efron B (1987) Better bootstrap confidence intervals. J Am Stat Assoc 82:171–185CrossRefGoogle Scholar
  46. Fyler CA (2011) An extremly hyperapolytic Acanthobothrium species (Cestoda: Tetraphyllidea) from the japanese wobbegong, Orectolobus japonicus (Elasmobranchii: Orectolobiformes) in Taiwan. Comp Parasitol 78:4–14CrossRefGoogle Scholar
  47. Fyler CA, Caira JN (2011) Phylogenetic status of four new species of Acanthobothrium (Cestoda : Tetraphyllidea) parasitic on the wedgefish Rhynchobatus laevis (Elasmobranchii : Rhynchobatidae): implications for interpreting host associations. Invertebr Syst 24:419–433CrossRefGoogle Scholar
  48. Fyler CA, Caira JN, Jensen K (2009) Five new species of Acanthobothrium (Cestoda: Tetraphyllidea) from an unusual species of Himantura (Rajiformes: Dasyatidae) from northern Australia. Folia Parasitol 56:107–128CrossRefPubMedGoogle Scholar
  49. Harper JT, Saunders GW (2001) The application of sequences of the ribosomal cistron to the systematics and classification of the florideophyte red algae (Florideophyceae, Rhodophyta). Cah Biol Mar 42:25–38Google Scholar
  50. Healy CJ, Caira JN, Jensen K, Webster BL, Littlewood DTJ (2009) Proposal for a new tapeworm order, Rhinebothriidea. Int J Parasitol 39:497–511CrossRefPubMedGoogle Scholar
  51. Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210CrossRefPubMedGoogle Scholar
  52. Hernandez AD, Sukhdeo MVK (2008) Parasites alter the topology of a stream food web across seasons. Oecologia 156:613–624CrossRefPubMedGoogle Scholar
  53. Holland ND, Wilson NG (2009) Molecular identification of larvae of a tetraphyllidean tapeworm (Platyhelminthes: Eucestoda) in a razor clam as an alternative intermediate host in the life cycle of Acanthobothrium brevissime. J Parasitol 95:1215–1217CrossRefPubMedGoogle Scholar
  54. Hudson P, Greenman J (1998) Competition mediated by parasites: biological and theoretical progress. Trends Ecol Evol 13:387–390CrossRefPubMedGoogle Scholar
  55. Huelsenbeck JP, Ronquist F (2001) MRBAYES. Bayesian Inference of phylogeny. Bioinformatics 17:754–755CrossRefPubMedGoogle Scholar
  56. Huxham M, Raffaelli D, Pike A (1995) Parasites and food web patterns. J Anim Ecol 64:168–176CrossRefGoogle Scholar
  57. Jensen K, Bullard SA (2010) Characterization of a diversity of tetraphyllidean and rhinebothriidean cestode larval types, with comments on host associations and life-cycles. Int J Parasitol 40:889–910CrossRefPubMedGoogle Scholar
  58. Jensen K, Caira JN, Cielocha JJ, Littlewood DTJ, Waeschenbach A (2016) When proglottids and scoleces conflict: phylogenetic relationships and a family-level classification of the Lecanicephalidea (Platyhelminthes: Cestoda). Int J Parasitol 46:291–310CrossRefPubMedGoogle Scholar
  59. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence date. Bioinformatics 28:1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
  60. Keeling CP, Burt MDB (1996) Echeneibothrium canadensis n. sp. (Tetraphyllidea: Phyllobothriidae) in the spiral intestine of the thorny skate (Raja radiata) from the Canadian Atlantic Ocean. Can J Zool 74:1590–1593CrossRefGoogle Scholar
  61. Klotz D, Hirzmann J, Bauer C, Schöne J, Iseringhausen M, Wohlsein P, Baumgartner W, Herder V (2018) Subcutaneous merocercoids of Clistobothrium sp. in two cape fur seals (Arctocephalus pusillus pusillus). Int J Parasitol Parasites Wildl 7:99–105CrossRefPubMedPubMedCentralGoogle Scholar
  62. Kodedová I, Doležel D, Broučková M, Jirků M, Hypša V, Lukeš J, Scholz T (2000) On the phylogenetic positions of the Caryophyllidea, Pseudophyllidea and Proteocephalidea (Eucestoda) inferred from 18S rRNA. Int J Parasitol 30:1109–1113CrossRefPubMedGoogle Scholar
  63. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefPubMedGoogle Scholar
  64. Kuris AM, Jaramillo AG, McLaughlin JP, Weinstein SB, Garcia-Vedrenne AE, Poinar GO Jr, Pickering M, Steinauer ML, Espinoza M, Ashford JE, Dunn GL (2015) Monsters of the sea serpent: parasites of an oarfish, Regalecus russellii. J Parasitol 101:41–44CrossRefPubMedGoogle Scholar
  65. Lafferty KD, Morris AK (1996) Altered behaviour of parasitized killifish increases susceptibility to predation by birds final hosts. Ecology 77:1390–1397CrossRefGoogle Scholar
  66. Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci 103:11211–11216CrossRefPubMedGoogle Scholar
  67. Laskowski Z, Rocka A (2014) Molecular identification larvae of Onchobothrium antarcticum (Cestoda: Tetraphyllidea) from marbled rockcod, Notothenia rossii, in Admiralty Bay (King George Island, Antarctica). Acta Parasitol 59:767–772CrossRefPubMedGoogle Scholar
  68. Littlewood DTJ (2011) Systematics as a cornerstone of parasitology: overview and preface. Parasitology 138:1633–1637CrossRefPubMedGoogle Scholar
  69. Lockyer AE, Olson PD, Littlewood DTJ (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biol J Linn Soc 78:155–171CrossRefGoogle Scholar
  70. Mariaux J (1998) A molecular phylogeny of the Eucestoda. J Parasitol 84:114–124CrossRefPubMedGoogle Scholar
  71. McMillan P, Francis M, James G, Paul L, Marriott P, Mackay E, Wood B, Griggs L, Sui H, Wei F (2011a) New Zealand fishes, volume 1: a field guide to common species caught by bottom and midwater fishing. New Zealand aquatic environment and biodiversity report no. 68. Ministry of Fisheries, WellingtonGoogle Scholar
  72. McMillan P, Griggs L, Francis M, Marriott P, Paul L, Mackay E, Wood B, Sui H, Wei F (2011b) New Zealand fishes. Volume 3: a field guide to common species caught by surface fishing. New Zealand aquatic environment and biodiversity report no. 69. Ministry of Fisheries, WellingtonGoogle Scholar
  73. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: proceedings of the gateway computing environments workshop (GCE). New Orleans, pp 18Google Scholar
  74. Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850CrossRefPubMedGoogle Scholar
  75. Naylor JR, Webber WR, Booth JD (2005) A guide to common offshore crabs in New Zealand waters. New Zealand aquatic environment and biodiversity report no. 2. Ministry of Fisheries, WellingtonGoogle Scholar
  76. Olson PD, Caira JN (1999) Evolution of the major lineages of tapeworms (Platyhelminthes: Cestoidea) inferred from 18S ribosomal DNA and elongation factor-1a. J Parasitol 85:1134–1159CrossRefPubMedGoogle Scholar
  77. Olson PD, Littlewood DTJ, Bray RA, Mariaux J (2001) Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Mol Phylogenet Evol 19:443–467CrossRefPubMedGoogle Scholar
  78. Olson PD, Poddubnaya LG, Littlewood DTJ, Scholz T (2008) On the position of Archigetes and its bearing on the early evolution of the tapeworms. J Parasitol 94:898–904CrossRefPubMedGoogle Scholar
  79. Olson PD, Caira JN, Jensen K, Overstreet RM, Palm HW, Beveridge I (2010) Evolution of the trypanorhynch tapeworms: parasite phylogeny supports independent lineages of sharks and rays. Int J Parasitol 40:223–242CrossRefPubMedGoogle Scholar
  80. Pace ML, Cole JJ, Carpenter SR, Kitchell JF (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol 14:483–488CrossRefPubMedGoogle Scholar
  81. Paine RT (1980) Food webs: linkage, interaction strength and community infrastructure. J Anim Ecol 49:667–685CrossRefGoogle Scholar
  82. Palm HW (2004) The Trypanorhyncha Diesing, 1863. PKSPL-IPB Press, BogorGoogle Scholar
  83. Palm HW, Waeschenbach A, Olson PD, Littlewood DT (2009) Molecular phylogeny and evolution of the Trypanorhyncha Diesing, 1863 (Platyhelminthes: Cestoda). Mol Phylogenet Evol 52:351–367CrossRefPubMedGoogle Scholar
  84. Parker GA, Chubb JC, Ball MA, Roberts GN (2003) Evolution of complex life cycles in helminth parasites. Nature 425:480–484CrossRefPubMedGoogle Scholar
  85. Pascual M, Dunne JA, Levin S (2005) Challenges for the future: integrating ecological structure and dynamics. In: Pascual M, Dunne JA (eds) Ecological networks: linking structure to dynamics in food webs. Oxford University Press, Oxford, pp 351–371Google Scholar
  86. Poulin R, Keeney DB (2008) Host specificity under molecular and experimental scrutiny. Trends Parasitol 24:24–28CrossRefPubMedGoogle Scholar
  87. Poulin R, Blasco-Costa I, Randhawa HS (2016) Integrating parasitology and marine ecology: seven challenges towards greater synergy. J Sea Res 113:3–10CrossRefGoogle Scholar
  88. Rambaut A, Drummond AJ, Suchard M (2014) tracer v1. 6 http://beast.bio.ed.ac.uk/Tracer
  89. Randhawa HS (2011) Insights into the lifecycle of a tapeworm infecting great white sharks using a molecular approach. J Parasitol 97:275–280CrossRefPubMedGoogle Scholar
  90. Randhawa HS, Brickle P (2011) Larval parasite gene sequence data reveal trophic links in the life cycles of porbeagle shark tapeworms. Mar Ecol Prog Ser 431:215–222CrossRefGoogle Scholar
  91. Randhawa HS, Burt MB (2008) Determinants of host specificity and comments on attachment site specificity of tetraphyllidean cestodes infecting rajid skates from the Northwest Atlantic. J Parasitol 94:436–461CrossRefPubMedGoogle Scholar
  92. Randhawa HS, Saunders GW, Burt MDB (2007) Establishment of the onset of host specificity in four phyllobothriid tapeworm species (Cestoda: Tetraphyllidea) using a molecular approach. Parasitology 134:1291–1300CrossRefPubMedGoogle Scholar
  93. Reiczigel J, Rózsa L (2005) Quantitative parasitology 3.0. Distributed by the authors, BudapestGoogle Scholar
  94. Reyda FB, Olson PD (2003) Cestodes of cestodes of Peruvian freshwater stingrays. J Parasitol 89:1018–1024CrossRefPubMedGoogle Scholar
  95. Ruhnke TR, Caira JN, Cox A (2015) The cestode order Rhinebothriidea no longer family-less: a molecular phylogenetic investigation with erection of two new families and description of eight new species of Anthocephalum. Zootaxa 3904:51–81CrossRefPubMedGoogle Scholar
  96. Sato T, Egusa T, Fukushima K, Oda T, Ohte N, Tokuchi N, Watanabe K, Kanaiwa M, Murakami I, Lafferty KD (2012) Nematomorph parasites indirectly alter the food web and ecosystem function of streams through behavioural manipulation of their cricket hosts. Ecol Lett 15:786–793CrossRefPubMedGoogle Scholar
  97. Scholz T, de Chambrier A, Kutcha R, Littlewood DTJ, Waeschenbach A (2013) Macrobothriotaenia ficta (Cestoda: Proteocephalidea), a parasite of sunbeam snake (Xenopeltis unicolor): example of convergent evolution. Zootaxa 3640:485–499CrossRefPubMedGoogle Scholar
  98. Scholz T, de Chambrier A, Shimazu T, Ermolenko A, Waeschenbach A (2016) Proteocephalid tapeworms (Cestoda: Onchoproteocephalidea) of loaches (Cobitoidea): evidence for monophyly and high endemism of parasites in the Far East. Parasitol Int 66:871–883CrossRefPubMedGoogle Scholar
  99. Thompson RM, Mouritsen KN, Poulin R (2005) Importance of parasites and their life cycle characteristics in determining the structure of a large marine food web. J Anim Ecol 74:77–85CrossRefGoogle Scholar
  100. Thompson RM, Poulin R, Mouritsen KN, Thieltges DW (2013) Resource tracking in marine parasites: going with the flow? Oikos 122:1187–1194CrossRefGoogle Scholar
  101. Tracey D, Anderson O, Clark M, Oliver M (2005) A guide to common deepsea invertebrates in New Zealand waters. New Zealand aquatic environment and biodiversity report no. 10. Ministry of Fisheries, WellingtonGoogle Scholar
  102. Waeschenbach A, Webster BL, Bray RA, Littlewood DTJ (2007) Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Mol Phylogenet Evol 45:311–325CrossRefPubMedGoogle Scholar
  103. Waeschenbach A, Webster BL, Littlewood DTJ (2012) Adding resolution to ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with large fragments of mtDNA. Mol Phylogenet Evol 63:834–847CrossRefPubMedGoogle Scholar
  104. Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513PubMedGoogle Scholar
  105. Williams HH (1961) Observations on Echeneibothrium maculatum (Cestoda:Tetraphyllidea). J Mar Biol Assoc UK 41:631–652CrossRefGoogle Scholar
  106. Wood CL, Byers JE, Cottingham KL, Altman I, Donahue MJ, Blakeslee AMH (2007) Parasites alter community structure. Proc Natl Acad Sci U S A 104:9335–9339CrossRefPubMedPubMedCentralGoogle Scholar
  107. Zehnder MP, Mariaux J (1999) Molecular systematic analysis of the order Proteocephalidea (Eucestoda) based on mitochondrial and nuclear rDNA sequences. Int J Parasitol 29:1841–1852CrossRefPubMedGoogle Scholar
  108. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Zoology DepartmentOtago UniversityDunedinNew Zealand
  2. 2.Ecology Degree ProgrammeOtago UniversityDunedinNew Zealand
  3. 3.Fisheries DepartmentFalkland Islands GovernmentStanleyFalkland Islands
  4. 4.South Atlantic Environmental Research InstituteStanleyFalkland Islands
  5. 5.New Brunswick MuseumSaint JohnCanada

Personalised recommendations