Softer rocks in the intertidal zones of southern Japan are occasionally excavated by the rock-boring sea urchin, Echinostrephus molaris, and the pits are often succeeded by non-boring sea urchins, Anthocidaris crassispina and Echinometra tsumajiro after the death of Ec. molaris. Although the rock-boring sea urchin can fold their thin spines and retreat deeply into the pit bottoms, non-boring sea urchins with stouter spines cannot retreat deeply, thus, leaving spaces between their spines and the pit wall. To evaluate the uniqueness of these pits as microhabitats, we conducted an extensive census of biota both inside and outside of the pits occupied by rock-boring and non-boring sea urchins in tidal pools at Shirahama in southern Japan (33°69′51″N, 135°33′58″E). Macrophytes were only observed outside the pits, whereas sessile filter feeders and detritus feeders were found at similar frequencies in all of the microhabitats. The abundance and species richness of algal grazers and carnivores, however, were significantly higher in outside and inside the pits occupied by non-boring sea urchins compared to pits occupied by rock-boring sea urchins. The pit occupied by a non-boring sea urchin was specifically inhabited by a limpet-like trochid snail, Broderipia iridescens, the biology of which is almost completely unknown. Our data suggest that this trochid species is the first example of obligate inquiline with a non-boring pit-inhabiting sea urchin, adapted to the life in the pits, where the limpet benefit by sneaking in the gap between the pit wall and sea urchin spines, escaping from contact with the spines and being protected from attack by predaceous muricid snails.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Bak RPM (1994) Sea urchin bioerosion on coral reefs: place in the carbonate budget and relevant variables. Coral Reefs 13:99–103
Campbell AC, Dart JK, Head SM, Ormond RF (1973) The feeding activity of Echinostrephus molaris (de Blainville) in the central Red Sea. Mar Freshwater Behav Physiol 2:155–169.
Carreiro-Silva M, McClanahan TR (2001) Echinoid bioerosion and herbivory on Kenyan coral reefs: the role of protection from fishing. J Exper Mar Biol Ecol 262:133–153
Davidson TM, Grupe BM (2014) Habitat modification in tidepools by bioeroding sea urchins and implications for fine-scale community structure. Mar Ecol 36:185–194
Davidson TM, Shanks AL, Rumrill SS (2010) The composition and density of fauna utilizing burrow microhabitats created by a non-native burrowing crustacean (Sphaeroma quoianum). Biol Invasion 12:1403–1413
Delongueville C, Scaillet R (2009) Illustration de Vitreolina philippi (Ponzi, de Rayneval & Van den Hecke, 1854) sur Paracentrotus lividus (Lamarck, 1816) à Chypre Nord. NOVAPEX/Société 10:100
Dumont CP, Lau DC, Astudillo JC, Fong KF, Chak ST, Qiu JW (2013) Coral bioerosion by the sea urchin Diadema setosum in Hong Kong: susceptibility of different coral species. J Exper Mar Biol Ecol 441:71–79
Gherardi F (1991) Eco-ethological aspects of the symbiosis between the shrimp Athanas indicus (Coutière 1903) and the sea urchin Echinometra mathaei (de Blainville 1825). Trop Zool 4:107–128
Harper E, Morton B (1997) Muricid predation upon an under-boulder community of epibyssate bivalves in the Cape D’Aguilar Marine Reserve, Hong Kong. The Marine Flora and Fauna of Hong Kong and Southern China IV. Hong Kong University Press, Hong Kong, pp 263–284
Hylleberg J (1994) Phylum Sipuncula. Part 2. Cryptic fauna with emphasis on sipunculans in hump coral Porites lutea, the Andaman Sea, Thailand. Phuket Mar Biol Cent Res Bull 59:33–41
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386
Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957
Killian CE, Metzler RA, Gong Y, Churchill TH, Olson IC, Trubetskoy V, Christensen MB, Fournelle JH, De Carlo F, Cohen S, Mahamid J, Scholl A, Young A, Doran A, Wilt FH, Coppersmith SN, Gilbert PUPA (2011) Self-sharpening mechanism of the sea urchin tooth. Adv Funct Mater 21:682–690
Kishu Shimanto Research Group (1972) The Muro Group in the Upperreaches of Koza River in Wakayama Prefecture: The study of the Shimanto Terrain in the Kii Peninsula, Southwest Japan (Part 5). Chikyukagaku (in Japanese) 26:195–204
Kobayashi N, Tokioka T (1976) Preliminary observatoin on the maturation of the burrowing sea urchin, Echinostrephus aciculatus (A. Agassiz), in the vicinity of Seto. Publ Seto Mar Biol Lab 23:57–62
Nakashima Y (1987) Reproductive strategies in a partially protandrous shrimp, Athanas kominatoensis (Decapoda: Alpheidae): sex change as the best of a bad situation for subordinates. J Ethol 5:145–159
Ohgaki SI, Komemoto KI, Funayama N (2011) 3. Comments on selected species. Publ Seto Mar Biol Lab. Spec Publ Ser 11:15–23
Parker GH (1936) An inquiline gammarid on the sea-urchin Lytechinus. Ecology 17:185–186
Schoppe S, Werding B (1996) The boreholes of the sea urchin genus Echinometra (Echinodermata: Echinoidea: Echinometridae) as a microhabitat in tropical South America. Mar Ecol 17:181–186
Solovjev AN, Markov AV (2013) The role of echinoids in shaping environments. Paleontol J 47:480–484
Valentich-Scott P, Dinesen GE (2004) Rock and coral boring Bivalvia (Mollusca) of the middle Florida Keys, USA. Malacologia 46:339–354
Williams ST, Donald KM, Spencer HG, Nakano T (2010) Molecular systematics of the marine gastropod families Trochidae and Calliostomatidae (Mollusca: Superfamily Trochoidea). Mol Phylogen Evol 54:783–809
Gordillo S (1998) Trophonid gastropod predation on recent bivalves from the Magellanic Region. Bivalves: an eon of evolution. Paleobiological Studies Honoring Norman D. Newell :251–254.
We thank all the staffs of the Seto Marine Biological Laboratory for supporting our field survey, Ryo Nakayama and Youhei Yamauchi of the Laboratory for technical support, and Kasumi Kondo of Kyoto University for helping with the sampling.
This work was supported by Grant-in-Aid for Scientific Research 2015–2019 (15H02420) to MK.
Conflict of interest
We have no conflict of interest.
Reviewed by Undisclosed experts.
Responsible Editor: S. Connell.
About this article
Cite this article
Yamamori, L., Kato, M. The macrobenthic community in intertidal sea urchin pits and an obligate inquilinism of a limpet-shaped trochid gastropod in the pits. Mar Biol 164, 61 (2017). https://doi.org/10.1007/s00227-017-3091-3
- Rock-boring sea urchin
- Ecosystem engineer
- Obligate commensalism
- Flattening of shell