Skip to main content

Host selection and ovipositor length in eight sympatric species of sculpins that deposit their eggs into tunicates or sponges

Abstract

Interspecific interactions between parasites and hosts can influence the evolution of behavioural and morphological adaptations of both parasites and their hosts. There is, however, little empirical evidence available regarding the evolution of reproductive traits driven by these interactions. In this paper, we investigated host selection and ovipositor length in nine sympatric marine sculpins that oviposit into tunicates or sponges. Field and genetic studies have revealed host use for eight out of nine species of sculpins investigated here: five species of Pseudoblennius, two species of Furcina and one species of Vellitor. For one species studied (V. minutus), no egg masses could be found. Ovipositor length reflects morphology of host species utilised: six sculpin species had extremely long ovipositors allowing females to attach eggs to the deep atrium of solitary tunicates, whereas the two species that attached their eggs to the small space of atrial siphon of colonial tunicates and the spongocoel of sponges had short ovipositors. Ovipositor length varied between solitary-tunicate spawners and species with longer ovipositors selected larger tunicates. Since the ancestral form is non-parasitic, the ovipositor evolved as an adaptation to utilise sponges and tunicates as hosts. Sculpins found sympatrically may show host specificity to avoid interspecific competition for spawning niches and ovipositors may have evolved depending on the species and size of host invertebrates.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Abe T, Munehara H (2009) Adaptation and evolution of reproductive mode in copulating cottoid species. In: Jamieson BGM (ed) Reproductive biology and phylogeny of fishes (agnathans and bony fishes). Science Publishers, Enfield, pp 221–246

    Chapter  Google Scholar 

  2. Akagawa I, Hara M, Iwamoto T (2008) Egg concealment in tunicates by females of the Japanese tubesnout, Aulichthys japonicus (Gasterosteiformes), and its subsequent copulation. Ichthyol Res 55:85–89

    Article  Google Scholar 

  3. Andersson M (1994) Sexual selection. Princeton Univ. Press, Princeton

    Google Scholar 

  4. Awata S (2015) Diversity and evolution of reproductive strategies in marine sculpins. Aquabiol 37:614–621

    Google Scholar 

  5. Awata S (2017) Taxonomic and ecological notes on marine sculpins on the coast of Sado Island in the Sea of Japan. Nat Hist Sado Isl 5:9–20

    Google Scholar 

  6. Balon EK (1975) Reproductive guilds of fishes—proposal and definition. J Fish Res Board Can 32:821–864

    Article  Google Scholar 

  7. Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic Press, London

    Google Scholar 

  8. Busby MS, Blood DM, Fleischer AJ, Nichol DG (2012) Egg deposition and development of eggs and larvae of bigmouth sculpin (Hemitripterus bolini). Northwest Nat 93:1–16

    Article  Google Scholar 

  9. Dunn CW, Giribet G, Edgecombe GD, Hejnol A (2014) Animal phylogeny and its evolutionary implications. Annu Rev Ecol Evol Syst 45:371–395

    Article  Google Scholar 

  10. Elias LG, Kjellberg F, Farache FHA, Almeida EAB, Rasplus J-Y, Cruaud A, Peng Y-Q, Yang D-R, Pereira RAS (2018) Ovipositor morphology correlates with life history evolution in agaonid fig wasps. Acta Oecol 90:109–116

    Article  Google Scholar 

  11. Gardner JR, Orr JW, Stevenson DE, Spies I, Somerton DA (2016) Reproductive parasitism between distant phyla: molecular identification of snailfish (Liparidae) egg masses in the gill cavities of king crabs (Lithodidae). Copeia 104:645–657

    Article  Google Scholar 

  12. Ghara M, Kundanati L, Borges RM (2011) Nature’s Swiss Army knives: ovipositor structure mirrors ecology in a multitrophic fig wasp community. PLoS One 6:e23642

    CAS  Article  Google Scholar 

  13. Hunter CJ (1969) Confirmation of symbiotic relationship between liparid fishes (Careproctus spp.) and male king crab (Paralithodes camtschatica). Pac Sci 23:546–547

    Google Scholar 

  14. Iwata A (1983) A revision of the cottid fish genus Vellitor. Jpn J Ichthyol 30:1–9

    Google Scholar 

  15. Keenleyside MHA (1991) Parental care. In: Keenleyside MHA (ed) Cichlid fishes: behaviour, ecology and evolution. Chapman and Hall, London, pp 191–208

    Google Scholar 

  16. Kimura S, Tsumoto K, Mori K (1987) Development of eggs, larvae and juveniles of the cottid fish, Pseudoblennius cottoides, reared in the laboratory. Jpn J Ichthyol 34:346–350

    Article  Google Scholar 

  17. Kimura S, Tsumoto K, Mori K (1988) Development of the cottid fish, Pseudoblennius percoides, reared in the laboratory, with brief descriptions of juvenile P. marmoratus and P. zonostigma. Jpn J Ichthyol 35:19–24

    Article  Google Scholar 

  18. Kitamura J (2005) Factors affecting seasonal mortality of rosy bitterling (Rhodeus ocellatus kurumeus) embryos on the gills of their host mussel. Popul Ecol 47:41–51

    Article  Google Scholar 

  19. Kitamura J (2007) Reproductive ecology and host utilization of four sympatric bitterling (Acheilognathinae, Cyprinidae) in a lowland reach of the Harai River in Mie, Japan. Environ Biol Fish 78:37–55

    Article  Google Scholar 

  20. Kitamura J, Nagata N, Nakajima J, Sota T (2012) Divergence of ovipositor length and egg shape in a brood parasitic bitterling fish through the use of different mussel hosts. J Evol Biol 25:566–573

    CAS  Article  Google Scholar 

  21. Knope ML (2013) Phylogenetics of the marine sculpins (Teleostei: Cottidae) of the North American Pacific Coast. Mol Phylogenet Evol 66:341–349

    Article  Google Scholar 

  22. Koya Y, Hayakawa Y, Markevich A, Munehara H (2011) Comparative studies of testicular structure and sperm morphology among copulatory and non-copulatory sculpins (Cottidae: Scorpaeniformes: Teleostei). Ichthyol Res 58:109–125

    Article  Google Scholar 

  23. Koya Y, Mitsuhashi N, Awata S, Ito T, Munehara H (2015) Identification of the reproductive mode for internal gamete association in Vellitor centropomus (Cottidae): gonadal histological analysis. Japan J Ichthyol 62:121–131

    Google Scholar 

  24. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  Article  Google Scholar 

  25. Le Ralec A, Rabasse JM, Wajnberg E (1996) Comparative morphology of the ovipositor of some parasitic Hymenoptera in relation to characteristics of their hosts. Can Entomol 128:413–433

    Article  Google Scholar 

  26. Leung TLF (2014) Fish as parasites: an insight into evolutionary convergence in adaptations for parasitism. J Zool 294:1–12

    Article  Google Scholar 

  27. Love DC, Shirley TC (1993) Parasitism of the golden king crab, Lithodes aequispinus Benedict, 1895, by a liparid fish. Crustaceana 65:97–104

    Article  Google Scholar 

  28. Mehbub MF, Lei J, Franco C, Zhang W (2014) Marine sponge derived natural products between 2001 and 2010: trends and opportunities for discovery of bioactives. Mar Drugs 12:4539–4577

    Article  Google Scholar 

  29. Mills SC, Reynolds JD (2002) Mussel ventilation rates as approximate cue for host selection by bitterling, Rhodeus sericeus. Oecologia 131:473–478

    Article  Google Scholar 

  30. Mills SC, Reynolds JD (2003) The bitterling-mussel interaction as a test case for co-evolution. J Fish Biol 63:84–104

    Article  Google Scholar 

  31. Momota K, Munehara H (2017) Reproductive ecology and morphological changes during the early life stages of Pallasina barbata (Steindachner, 1876). Bull Fish Sci Hokkaido Univ 67:7–12

    Google Scholar 

  32. Munehara H (1991) Utilization and ecological benefits of a sponge as a spawning bed by the little dragon sculpin Blepsias cirrhosis. Jpn J Ichthyol 38:179–184

    Google Scholar 

  33. Munehara H, Takano K, Koya Y (1989) Internal gametic association and external fertilization in the elkhorn sculpin, Alcichthys alcicornis. Copeia 1989:673–678

    Article  Google Scholar 

  34. Munehara H, Goto A, Yabe M (2011) Diversity of cottoid fishes—adaptation and evolution. Tokai Univ Press, Kanagawa

    Google Scholar 

  35. Nakabo T, Kai Y (2013) Cottidae. In: Nakabo T (ed) Fishes of Japan with pictorial keys to the species, 3rd edn. Tokai University Press, Hadano, pp 1160–1188

    Google Scholar 

  36. Nelson JS, Grande TC, Wilson MVH (2016) Fishes of the World, 5th edn. Wiley, East Orange

    Book  Google Scholar 

  37. Nishida T, Inui R, Onikura N (2008) A note on the spawning bed of Pseudoblennius percoides (Scorpaeniformes, Cottidae) in shallow sea areas around coastal Fukutsu, northern Kyusyu Island, Japan. Biogeography 10:45–51

    Google Scholar 

  38. Okamura O, Amaoka K (eds) (1997) Seawater fishes in Japan. Yamatokeikoku-sha, Tokyo

    Google Scholar 

  39. Palumbi SR (1996) What can molecular genetics contribute to marine biogeography? An urchin’s tale. J Exp Mar Biol Ecol 203:75–92

    CAS  Article  Google Scholar 

  40. Paul VJ, Puglisi MP (2004) Chemical mediation of interactions among marine organisms. Nat Prod Rep 21:189–209

    CAS  Article  Google Scholar 

  41. Paul VJ, Puglisi MP, Ritson-Williams R (2006) Marine chemical ecology. Nat Prod Rep 23:153–180

    CAS  Article  Google Scholar 

  42. Peden AE, Corbett CA (1973) Commensalism between a liparid fish, Careproctus sp., and the lithodid box crab, Lopholithodes foraminatus. Can J Zool 51:555–556

    Article  Google Scholar 

  43. Poltev YN, Mukhametov IN (2009) Concerning the problem of carcinophilia of Careproctus species (Scorpaeniformes: Liparidae) in the North Kurils. Russ J Mar Biol 35:215–223

    Article  Google Scholar 

  44. Reichard M, Ondrackova M, Przybylski M, Liu H, Smith C (2006) The costs and benefits in an unusual symbiosis: experimental evidence that bitterling fish (Rhodeus sericeus) are parasites of unionid mussels in Europe. J Evol Biol 19:788–796

    CAS  Article  Google Scholar 

  45. Reichard M, Liu H, Smith C (2007) The co-evolutionary relationship between bitterling fishes and freshwater mussels: insights from interspecific comparisons. Evol Ecol Res 9:239–259

    Google Scholar 

  46. Schmidt TR, Gold JR (1993) Complete sequence of the mitochondrial cytochrome b gene in the cherryfin shiner, Lythrurus roseipinnis (Teleostei: Cyprinidae). Copeia 1993:880–883

    Article  Google Scholar 

  47. Shinomiya A (1985) Studies on the reproductive physiology and ecology in three marine cottid fish. Dissertation, Hokkaido University

  48. Shinomiya A, Ikemoto M (1987) Spawning habits of the sculpin Pseudoblennius percoides in relation to sea squirt. In: Advance abstracts for the 20th annual meeting, The Ichthyological Society of Japan

  49. Shiogaki M, Dotsu Y (1974) The spawning of the sea sculpin, Pseudoblennius cottoides. Bull Fac Fish Nagasaki Univ 38:71–76

    Google Scholar 

  50. Smith C, Rippon K, Douglas A, Jurajda P (2001) A proximate cue for oviposition site choice in the bitterling (Rhodeus sericeus). Freshw Biol 46:903–911

    Article  Google Scholar 

  51. Smith C, Reichard M, Jurajda P, Przybylski M (2004) The reproductive ecology of the European bitterling (Rhodeus sericeus). J Zool 262:107–124

    Article  Google Scholar 

  52. Somerton DA, Donaldson W (1998) Parasitism of the golden king crab, Lithodes aequispinus, by two species of snailfish, genus Careproctus. Fish Bull 96:871–884

    Google Scholar 

  53. Spence R, Smith C (2013) Rose bitterling (Rhodeus ocellatus) embryos parasitize freshwater mussels by competing for nutrients and oxygen. Acta Zool 94:113–118

    Article  Google Scholar 

  54. Stoecker D (1980) Chemical defenses of ascidians against predators. Ecology 61:1327–1334

    CAS  Article  Google Scholar 

  55. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Uchida K (1932) Fish laying eggs in the body of tunicates. Kagaku 2:56–57

    Google Scholar 

  57. Uchida K (1979) Chigyo Wo Motomete. Iwanamisyoten, Tokyo

    Google Scholar 

  58. Uryu T (2011) Marine fishes of Izu. Kaiyusha, Tokyo

    Google Scholar 

  59. Yabe M (1985) Comparative osteology and myology of the superfamily Cottoidea (Pisces: Scorpaeniformes), and its phylogenetic classification. Mem Fac Fish Hokkaido Univ 32:1–130

    Google Scholar 

Download references

Acknowledgements

We thank Teruaki Nishikawa and Yuji Ise for help with the classification of tunicates and sponges. We are also grateful to Mitsuo Homma (Diving Service F. Wave), Ryo Honma (Sado Diving Centre), Yoshihisa Sato (Senkakuwan Ageshima Aquarium), Akihiro Yamada, Hiromitsu Takashima (Ogi Diving Centre), Tadashi Shoji (Diving Service S. World), Sadogashima SCUBA Diving Association and Kitakoura Recreational Fishing Cooperative for support in the field. We would like to thank Tomonobu Uryu for creating videos for us and Editage (http://www.editage.jp) for English language editing. The anonymous reviewers provided helpful comments on the manuscript. The project was financially supported in part by JSPS KAKENHI Grant Numbers JP24770016 and JP16H04841 to S.A., JP26450259 to Y.K. and JP25304011 to H.M. and by the Sasaki Environment Technology Foundation (H26) to S.A.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Satoshi Awata.

Ethics declarations

Ethical statement

The research reported in this study was carried out in accordance with Animal Care and Use Committees at Niigata University and Osaka City University. All of the procedures described above meet the ABS/ASAB guidelines for the ethical treatment of animals. Research permission was obtained from Fisheries Cooperative Association of Sado, Japan.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Reviewed by Undisclosed experts.

Responsible Editor: C. Eizaguirre.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Movie S1 Spawning behaviours of female Pseudoblennius cottoides in the aquarium. Six Halocynthia ritteri on wire-netting were placed in a 75 × 45 × 45 cm aquarium. Eggs were deposited in the atrium of a tunicate through the atrial siphon using extremely long ovipositors. Eggs were probably released into the atrium when the female opened her mouth. The female stayed still on the tunicate after spawning. She ejected her ovipositor 1 min 22 sec and left the tunicate 2 min 34 sec after the insert, respectively (not shown). This movie was filmed by H. S. on Feb. 7, 2015. Fish and tunicates were collected on the coast of Sado Island in the Sea of Japan. (M4V 7441 kb)

Movie S2 Failure of spawning by female Pseudoblennius cottoides in the aquarium. The atrial siphon of the tunicate closed before the sculpin female inserted her ovipositor. Settings were the same as in Movie S1. This movie was filmed by H. S. on Feb. 1, 2015. (M4V 5619 kb)

Movie S3 Spawning behaviours of female Pseudoblennius marmoratus in the field. Eggs were deposited in the spongocoel of a sponge using short ovipositors. This movie was filmed by Tomonobu Uryu on Dec. 28, 2009 at Izu Oceanic Park, Izu Peninsula, Pacific coast of Japan. Water temperature was about 16 °C and water depth was about 5 m. (M4V 11238 kb)

Supplementary material 1 (PDF 2266 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Awata, S., Sasaki, H., Goto, T. et al. Host selection and ovipositor length in eight sympatric species of sculpins that deposit their eggs into tunicates or sponges. Mar Biol 166, 59 (2019). https://doi.org/10.1007/s00227-019-3506-4

Download citation