Hostname: page-component-76fb5796d-qxdb6 Total loading time: 0 Render date: 2024-04-26T15:28:21.044Z Has data issue: false hasContentIssue false

Effect of a cold event on population and community of pit-inhabiting sea urchins in Western Pacific coasts

Published online by Cambridge University Press:  09 December 2021

Luna Yamamori*
Affiliation:
Seto Marine Biological Laboratory, Field Science Education and Research Center, Kyoto University, 459 Shirahama, Nishimuro, Wakayama, 649-2211, Japan
Makoto Kato
Affiliation:
Graduate School of Human and Environmental Studies, Kyoto University, Sakyo, Kyoto, 606-8313, Japan
*
Author for correspondence: Luna Yamamori, E-mail: strobilation980@gmail.com

Abstract

Coastal tide pools in southern Japan are inhabited by the rock-boring sea urchin Echinostrephus molaris, which excavate pits in the substrate. These pits are subsequently used by non-boring sea urchins such as Anthocidaris crassispina and Echinometra sp. B, and the recolonized pits are often inhabited by a commensal limpet-like trochid snail species, Broderipia iridescens. We explored the population and community dynamics of these sea urchins and the limpet-like snail by monitoring occupancy of 512 pits in tide pools in Shirahama, Japan from May 2017–May 2019. Initially, nearly all pits were occupied by any one of the three sea urchin species, but an unusual cold event in February 2018 caused a mass die off of these sea urchins. After this event, occupancy decreased from 99% to 15%, and the tropical species Echinometra sp. B disappeared from the study pools. We observed slow population recovery of E. molaris and A. crassispina, provably via migration of sub-adults from the subtidal zone. Turnover rate of the pit-occupying sea urchin species was <1.0% before the cold event, but drastically increased after the cold event. Population size of the commensal snail decreased along with those of their host, but the rate of commensalism was constant at 50–55% throughout the study period, suggesting that these snails followed their host sea urchins repeating inter-pit migration. Despite mass mortality and slow recovery, the sea urchin density remained high enough to maintain persistent sea urchin barrens throughout the study period.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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

Barnes, DKA, Crook, A, O'Mahoney, M, Steele, S and Maguire, D (2001) Sea temperature variability and Paracentrotus lividus (Echinoidea) population fluctuations. Journal of the Marine Biological Association of the United Kingdom 81, 359360.CrossRefGoogle Scholar
Barnes, DKA, Verling, E, Crook, A, Davidson, I and O'Mahoney, M (2002) Local population disappearance follows (20 yr after) cycle collapse in a pivotal ecological species. Marine Ecology Progress Series 226, 311313.CrossRefGoogle Scholar
Brothers, CJ, Harianto, J, McClintock, JB and Byrne, M (2016) Sea urchins in a high-CO2 world: the influence of acclimation on the immune response to ocean warming and acidification. Proceedings of the Royal Society B–Biological Sciences 283. https://doi.org/10.1098/rspb.2016.1501.CrossRefGoogle Scholar
Campbell, AC, Dart, JK, Head, SM and Ormond, RF (1973) The feeding activity of Echinostrephus molaris (de Blainville) in the central Red Sea. Marine and Freshwater Behaviour and Physiology 2, 155169.CrossRefGoogle Scholar
Chanket, W and Wangkulangkul, K (2019) Role of the sea urchin Stomopneustes variolaris (Lamarck, 1816) pits as a habitat for epilithic macroinvertebrates on a tropical intertidal rocky shore. Zoological Science 36, 330338.CrossRefGoogle ScholarPubMed
Fernandez, C, Caltagirone, A and Johnson, M (2001) Demographic structure suggests migration of the sea urchin Paracentrotus lividus in a coastal lagoon. Journal of the Marine Biological Association of the United Kingdom 81, 361362.CrossRefGoogle Scholar
Filbee-Dexter, K and Scheibling, RE (2014) Sea urchin barrens as alternative stable states of collapsed kelp ecosystems. Marine Ecology Progress Series 495, 125.CrossRefGoogle Scholar
Filbee-Dexter, K, Fredriksen, S, Norderhaug, KM, Rinde, E, Kristiansen, T, Albretsen, J and Wernberg, T (2020) Carbon export is facilitated by sea urchins transforming kelp detritus. Oecologia 192, 213225.CrossRefGoogle ScholarPubMed
Hernández, JC, Clemente, S, Sangil, C and Brito, A (2008) The key role of the sea urchin Diadema aff. antillarum in controlling macroalgae assemblages throughout the Canary Islands (eastern subtropical Atlantic): a spatio-temporal approach. Marine Environmental Research 66, 259270.CrossRefGoogle ScholarPubMed
Iwao, SI and Kuno, E (1968) Use of the regression of mean crowding on mean density for estimating sample size and the transformation of data for the analysis of variance. Population Ecology 10, 210214.CrossRefGoogle Scholar
Johnson, CR, Ling, S, Ross, D, Shepherd, S and Miller, K (2005) Establishment of the long–spined sea urchin (Centrostephanus rodgersii) in Tasmania: first assessment of potential threats to fisheries. https://eprints.utas.edu.au/6290/.Google Scholar
Kobayashi, N and Tokioka, T (1976) Preliminary observation on the maturation of the burrowing sea urchin, Echinostrephus aciculatus (A. Agassiz), in the vicinity of Seto. Publication of Seto Marine Biological Laboratory 23, 5762.CrossRefGoogle Scholar
Ling, SD and Johnson, CR (2009) Population dynamics of an ecologically important range-extender: kelp beds vs sea urchin barrens. Marine Ecology Progress Series 374, 113125.CrossRefGoogle Scholar
Ling, SD, Scheibling, RE, Rassweiler, A, Johnson, CR, Shears, N, Connell, SD, Salomon, AK, Norderhaug, KM, Pérez–Matus, A, Hernández, JC, Clemente, S, Blamey, LK, Hereu, B, Ballesteros, E, Sala, E, Garrabou, J, Cebrian, E, Zabala, M, Fujita, D and Johnson, LE (2015) Global regime shift dynamics of catastrophic sea urchin overgrazing. Philosophical Transactions of the Royal Society B–Biological Sciences 370. https://doi.org/10.1098/rstb.2013.0269.CrossRefGoogle Scholar
Mii, H (1962) Coastal geology of Tanabe Bay. The Science Reports of the Tohoku University. Second series. Geology 34, 56.Google Scholar
Moses, CS and Bonem, RM (2001) Recent population dynamics of Diadema antillarum and Tripneustes ventricosus along the north coast of Jamaica, WI. Bulletin of Marine Science 68, 327336.Google Scholar
Ohgaki, SI, Kato, T, Kobayashi, N, Tanase, H, Kumagai, NH, Ishida, S, Nakano, T, Wada, Y and Yusa, Y (2019) Effects of temperature and red tides on sea urchin abundance and species richness over 45 years in southern Japan. Ecological Indicators 96, 684693.CrossRefGoogle Scholar
Russo, AR (1980) Bioerosion by two rock boring echinoids (Echinometra mathaei and Echinostrephus aciculatus) on Enewetak Atoll, Marshall Islands. Journal of Marine Research 38, 99110.Google Scholar
Sala, E (1997) Fish predators and scavengers of the sea urchin Paracentrotus lividus in protected areas of the north-west Mediterranean Sea. Marine Biology 129, 531539.CrossRefGoogle Scholar
Sivertsen, K (1997) Geographic and environmental factors affecting the distribution of kelp beds and barren grounds and changes in biota associated with kelp reduction at sites along the Norwegian coast. Canadian Journal of Fisheries and Aquatic Sciences 54, 28722887.CrossRefGoogle Scholar
Stebbins, TD (1989) Population dynamics and reproductive biology of the commensal isopod Colidotea rostrata (Crustacea, Isopoda, Idoteidae). Marine Biology 101, 329337.CrossRefGoogle Scholar
Steneck, RS, Graham, MH, Bourque, BJ, Corbett, D, Erlandson, JM, Estes, JA and Tegner, MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental Conservation 29, 436459.CrossRefGoogle Scholar
Tokioka, T (1963) Supposed effects of the cold weather of the winter 1962–63 upon the intertidal fauna in the vicinity of Seto. Publication of Seto Marine Biological Laboratory 11, 415424.CrossRefGoogle Scholar
Tokioka, T (1966) Recovery of the Echinometra population in the intertidal zone in the vicinity of Seto, with a preliminary note on the mass mortality of some sea urchins in the summer season. Publication of Seto Marine Biological Laboratory 14, 716.CrossRefGoogle Scholar
Yamamori, L and Kato, M (2017) The macrobenthic community in intertidal sea urchin pits and an obligate inquilinism of a limpet-shaped trochid gastropod in the pits. Marine Biology 164. doi: 10.1007/s00227-017-3091-3.CrossRefGoogle Scholar
Yamamori, L and Kato, M (2018) Morphological and ecological adaptation of limpet-shaped top shells (Gastropoda: Trochidae: Fossarininae) to wave-swept rock reef habitats. PLoS ONE 13. https://doi.org/10.1371/journal.pone.0197719.CrossRefGoogle ScholarPubMed
Yusa, Y and Yamamoto, T (1994) Inside or outside the pits: variable mobility in conspecific sea urchin, Anthocidaris crassispina (A. Agassiz). Publications of the Seto Marine Biological Laboratory 36, 255266.CrossRefGoogle Scholar
Supplementary material: Image

Yamamori and Kato supplementary material

Yamamori and Kato supplementary material 1

Download Yamamori and Kato supplementary material(Image)
Image 1.9 MB
Supplementary material: Image

Yamamori and Kato supplementary material

Yamamori and Kato supplementary material 2

Download Yamamori and Kato supplementary material(Image)
Image 307.9 KB