Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-15T15:19:20.916Z Has data issue: false hasContentIssue false
  • English
  • Français

Predation behaviour of millimetre-sized hydrozoan polyps on early ivory shell juveniles

Published online by Cambridge University Press:  08 September 2020

Yulin Huang ,
Jingqiang Fu ,
Yutong Shi ,
Yunan Wang ,
Qi Cui  and
Xikun Song Open the ORCID record for Xikun Song [Opens in a new window]
Yulin Huang
Affiliation:
State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, 4221 South Xiang'an Road, Xiamen, 361102, China
Jingqiang Fu
Affiliation:
State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, 4221 South Xiang'an Road, Xiamen, 361102, China
Yutong Shi
Affiliation:
State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, 4221 South Xiang'an Road, Xiamen, 361102, China
Yunan Wang
Affiliation:
State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, 4221 South Xiang'an Road, Xiamen, 361102, China
Qi Cui
Affiliation:
State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, 4221 South Xiang'an Road, Xiamen, 361102, China
Xikun Song*
Affiliation:
State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, 4221 South Xiang'an Road, Xiamen, 361102, China
*
Author for correspondence: Xikun Song, E-mail: xksong@xmu.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Marine hydroids, the polyp stage of hydrozoans, are assumed to be carnivores and play an important role in benthic-pelagic coupling processes by regulating zooplankton populations and transferring energy. The known hydroid diets mainly consist of zooplankton as well as some benthic diatoms and metazoans, almost all of which have smaller dimensions than the polyp. In the present study, a large-scale breeding failure of the early juveniles of the ivory shell Babylonia areolata (Mollusca: Gastropoda: Babyloniidae) was found in a local aquaculture farm in Fujian, China in July 2018. About 640,000 out of 800,000 early juveniles (80%) died due to predation by a millimetre-sized colonial hydroid species that was initially overlooked. The hydrozoan species was identified as Eirene sp. (Cnidaria: Hydrozoa: Eirenidae) via the integration of morphological and molecular data. A laboratory feeding experiment showed that the hydroid predation led to an overall mortality of ivory shell juveniles of up to 92.6% after 48 h. The predation process was observed in the laboratory and a video showing the entire process was prepared. This is the first report of hydroids preying on gastropod juveniles, revealing a previously unknown threat to mollusc aquaculture including ivory shells. Several management practices are suggested to mitigate this newly recognized threat.

Keywords

AquacultureBabylonia areolatacaptive breedingEirenefeeding behaviour
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 100 , Issue 6 , September 2020 , pp. 889 - 895
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barange, M (1988) Prey selection and capture strategies of the benthic hydroid Eudendrium racemosum. Marine Ecology Progress Series 47, 83–88.10.3354/meps047083CrossRefGoogle Scholar
Barange, M and Gili, JM (1988) Feeding cycles and prey capture in Eudendrium racemosum (Cavolini, 1785). Journal of Experimental Marine Biology and Ecology 115, 281–293.10.1016/0022-0981(88)90160-8CrossRefGoogle Scholar
Bouillon, J, Boero, F and Seghers, G (1988) Notes additionelles sur les Hydroméduses de la mer de Bismarck (Hydrozoa-Cnidaria) II. Indo-Malayan Zoology 5, 87–99.Google Scholar
Bouillon, J, Gravili, C, Pagès, F, Gili, JM and Boero, F (2006) An introduction to Hydrozoa. Mémoires du Muséum National d'Histoire Naturelle 194, 1–591.Google Scholar
Brinckmann-Voss, A (1973) The life-cycle of Eirene lactea (Mayer, 1900) and Helgicirrha schulzei Hartlaub, 1909 (Phylum Cnidaria, Class Hydrozoa, Order Leptomedusae, Family Eirenidae). Publications of the Seto Marine Biological Laboratory 20, 63–72.10.5134/175790CrossRefGoogle Scholar
Chen, Y, Ke, C, Zhou, S and Li, F (2004) Embryonic and larval development of Babylonia formosae Habei (Altena and Gittenberger, 1981) (Gastropoda: Buccinidae) on China's coast. Acta Oceanologica Sinica 23, 521–531.Google Scholar
Christensen, HE (1967) Ecology of Hydractinia echinata (Fleming) (Hydroidea, Athecata) I. Feeding biology. Ophelia 4, 245–275.10.1080/00785326.1967.10409623CrossRefGoogle Scholar
Clark, SD and Cook, CB (1986) Inhibition of nematocyst discharge during feeding in the colonial hydroid Halocordyle disticha (=Pennaria tiarella): the role of previous prey-killing. Biological Bulletin 171, 405–416.10.2307/1541682CrossRefGoogle Scholar
Coma, R, Gili, JM and Zabala, M (1995) Trophic ecology of a benthic marine hydroid, Campanularia everta. Marine Ecology Progress Series 119, 211–220.10.3354/meps119211CrossRefGoogle Scholar
Cunha, AF, Collins, AG and Marques, AC (2017) Phylogenetic relationships of Proboscoida broch, 1910 (Cnidaria, Hydrozoa): are traditional morphological diagnostic characters relevant for the delimitation of lineages at the species, genus, and family levels? Molecular Phylogenetics and Evolution 106, 118–135.10.1016/j.ympev.2016.09.012CrossRefGoogle ScholarPubMed
Di Camillo, CG, Betti, F, Bo, M, Martinelli, M, Puce, S, Vasapollo, C and Bacestrello, G (2012) Population dynamics of Eudendrium racemosum (Cnidaria, Hydrozoa) from the North Adriatic Sea. Marine Biology 159, 1593–1609.10.1007/s00227-012-1948-zCrossRefGoogle Scholar
Fitridge, I, Dempster, T, Guenther, J and de Nys, R (2012) The impact and control of biofouling in marine aquaculture: a review. Biofouling 28, 649–669.10.1080/08927014.2012.700478CrossRefGoogle ScholarPubMed
Fitridge, I and Keough, M (2013) Ruinous resident: the hydroid Ectopleura crocea negatively affects suspended culture of the mussel Mytilus galloprovincialis. Biofouling: The Journal of Bioadhesion and Biofilm Research 29, 119–131.10.1080/08927014.2012.752465CrossRefGoogle ScholarPubMed
Genzano, GN (2005) Trophic ecology of a benthic intertidal hydroid, Tubularia crocea, at Mar del Plata, Argentina. Journal of the Marine Biological Association of the United Kingdom 85, 307–312.10.1017/S0025315405011197hCrossRefGoogle Scholar
Gili, JM and Hughes, RG (1995) The ecology of marine benthic hydroids. Oceanography Marine Biology: An Annual Review 33, 351–426.Google Scholar
Gili, JM, Hughes, RG and Alvà, V (1996 a) A quantitative study of feeding by the hydroid Tubularia larynx Ellis and Solander, 1786. Scientia Marina 60, 43–54.Google Scholar
Gili, JM, Alvà, V, Pagès, F, Klöser, H and Arntz, WE (1996 b) Benthic diatoms as the major food source in the sub-Antarctic marine hydroid Silicularia rosea. Polar Biology 16, 507–512.10.1007/BF02329070CrossRefGoogle Scholar
Gili, JM, Duró, A, García-Valero, J, Gasol, JM and Rossi, S (2008) Herbivory in small carnivores: benthic hydroids as an example. Journal of the Marine Biological Association of the United Kingdom 88, 1541–1546.10.1017/S0025315408003214CrossRefGoogle Scholar
Günzl, H (1984) “Siamesische” Zwillinge bei einer Hydromeduse. Mikrokosmos 73, 165–166.Google Scholar
Kubota, S (1979) Occurrence of a commensal hydroid Eugymnanthea inquilina Palombi from Japan. Journal of the Faculty of Science Hokkaido University Series VI Zoology 21, 396–406.Google Scholar
Kubota, S (1992) Four bivalve-inhabiting hydrozoans in Japan differing in range and host preference. Scientia Marina 56, 149–159.Google Scholar
Lü, W, Ke, C, Fu, J, You, W, Luo, X, Huang, M and Yu, J (2016) Evaluation of crosses between two geographic populations of native Chinese and introduced Thai spotted ivory shell, Babylonia areolata, in southern China. Journal of the World Aquaculture Society 47, 4.10.1111/jwas.12290CrossRefGoogle Scholar
Maggioni, D, Stefania, P, Galli, P, Seveso, D and Montano, S (2017) Description of Turritopsoides marhei sp. nov. (Hydrozoa, Anthoathecata) from the Maldives and its phylogenetic position. Marine Biology Research 13, 983–992.10.1080/17451000.2017.1317813CrossRefGoogle Scholar
Miglietta, MP, Tommasa, LD, Denitto, F, Gravili, C, Pagliara, P, Bouillon, J and Boero, F (2000) Approaches to the ethology of hydroids and medusae (Cnidaria, Hydrozoa). Scientia Marina 64, 63–71.10.3989/scimar.2000.64s163CrossRefGoogle Scholar
Mladineo, I, Petrić, M, Hrabar, J, Bočina, I and Peharda, M (2012) Reaction of the mussel Mytilus galloprovincialis (Bivalvia) to Eugymnanthea inquilina (Cnidaria) and Urastoma cyprinae (Turbellaria) concurrent infestation. Journal of Invertebrate Pathology 110, 118–125.10.1016/j.jip.2012.03.001CrossRefGoogle ScholarPubMed
Musco, L, Fernández, TV, Caroselli, E, Roberts, JM and Badalamenti, F (2018) Protocooperation among small polyps allows the coral Astroides calycularis to prey on large jellyfish. Ecology 99, 2400–2401.Google ScholarPubMed
Orejas, C, Gili, JM, López-González, PJ and Arntz, WE (2001) Feeding strategies and diet composition of four Antarctic cnidarian species. Polar Biology 24, 620–627.10.1007/s003000100272CrossRefGoogle Scholar
Orejas, C, Rossi, S, Peralba, À, García, E, Gili, JM and Lippert, H (2013) Feeding ecology and trophic impact of the hydroid Obelia dichotoma in the Kongsfjorden (Spitsbergen, Arctic). Polar Biology 36, 61–72.Google Scholar
Orlov, D (1996). Observations on the White Sea hydroid, Sarsia producta (Wright, 1858) (Hydrozoa: Athecata). Sarsia 81, 329–338.10.1080/00364827.1996.10413630CrossRefGoogle Scholar
Peng, J, Ge, X, Li, M, Zhou, W, Zhao, Q, Xu, P and Xie, J (2011) Study on Haplosporidium disease on Babylonia areolata. Acta Hydrobiologica Sinica 35, 803–807.Google Scholar
Piraino, S (1992) Halocoryne epizoica (Cnidaria: Hydrozoa) a hydroid that “bites”. Scientia Marina 56, 141–147.Google Scholar
Puce, S, Bavestrello, G, Arillo, A, Azzini, F and Cerrano, C (2002) Morpho-functional adaptation to suspension feeding in Eudendrium (Cnidaria, Hydrozoa). Italian Journal of Zoology 69, 301–304.10.1080/11250000209356473CrossRefGoogle Scholar
Rushforth, NB and Hofman, F (1972) Behavioral and electrophysiological studies of Hydra. III. Components of feeding behavior. Biological Bulletin 142, 110–131.10.2307/1540250CrossRefGoogle Scholar
Schuchert, P (2018) DNA barcoding of some Pandeidae species (Cnidaria, Hydrozoa, Anthoathecata). Reviue Suisse de Zoologie 125, 101–127.Google Scholar
Schuchert, P (2019) The hydroid of the medusa Lizzia blondina Forbes, 1848. Marine Biodiversity 49, 1683–1693.10.1007/s12526-019-00936-0CrossRefGoogle Scholar
Song, X (2006) Regeneration and settlement of two marine hydroids (Master thesis). Xiamen University, Xiamen, China.Google Scholar
Song, X, Gravili, C, Wang, J, Deng, Y, Wang, Y, Fang, L, Lin, H, Wang, S, Zheng, Y and Lin, J (2016). A new deep-sea hydroid (Cnidaria: Hydrozoa) from the Bering Sea Basin reveals high genetic relevance to Arctic and adjacent shallow-water species. Polar Biology 39, 461–471.10.1007/s00300-015-1793-xCrossRefGoogle Scholar
Song, X, Gravili, C, Ruthensteiner, B, Lyu, M and Wang, J (2018). Incongruent cladistics reveal a new hydrozoan genus (Cnidaria: Sertularellidae) endemic to the eastern and western coasts of the North Pacific Ocean. Invertebrate Systematics 32, 1083–1101.10.1071/IS17070CrossRefGoogle Scholar
Wang, J, Wang, R, Su, Y, Wu, K, Guo, Z, Jiang, J, Liu, G and Zhao, W (2013) Pathogen and pathology of “acute death syndrome” of Babylonia areolata. South China Fisheries Science 9, 93–99.10.3724/SP.J.1118.2013.00093CrossRefGoogle Scholar
Zheng, L, He, J, Lin, Y, Cao, W and Zhang, W (2014) 16S rRNA is a better choice than COI for DNA barcoding hydrozoans in the coastal waters of China. Acta Oceanologica Sinica 33, 55–76.10.1007/s13131-014-0415-8CrossRefGoogle Scholar

Huang et al. supplementary material

Huang et al. supplementary material 1

Download Huang et al. supplementary material(Video)
Video 20.1 MB
Supplementary material: Image

Huang et al. supplementary material

Huang et al. supplementary material 2

Download Huang et al. supplementary material(Image)
Image 11.2 MB
Supplementary material: File

Huang et al. supplementary material

Huang et al. supplementary material 3

Download Huang et al. supplementary material(File)
File 24.3 KB