Abstract
Ocean acidification (OA) is predicted to decrease the abundance of calcified organisms such as gastropods. Since hermit crabs utilize gastropod shell as mobile shelter, OA has indirect impacts on hermit crab population. To examine the impacts of OA on hermit crab communities, which use calcified shell as the mobile shelter, we conducted field surveys and laboratory experiments using volcanic CO2 seeps in Shikine Island, Japan. By comparing hermit crab community structures and shell availability among five intertidal rocky shores with different degrees of acidification, Paguroidea abundance and species richness were simplified in acidified areas. Rearing experiments comparing survival rates of two Paguroidea species, Pagurus filholi (de Man, 1887) and Clibanarius virescens (Krauss, 1843), at both adult and larval stages, between acidified and ambient aquaria revealed that acidified seawater reduced larval survival rate of C. virescens. Overall, the results indicated that the species-specific direct effect in elevated C. virescens larval mortality could simplify the Paguroidea species composition. In addition, such direct effect would also lead to reduction of Paguroidea abundance, along with indirect effects though a decrease in shell availability.
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Change history
28 August 2019
Figure 2 has been published incorrectly in the original publication of the article.
References
Agostini S, Wada S, Kon K, Omori A, Kohtsuka H, Fujimura H, Tsuchiya Y, Sato T, Shinagawa H, Yamada Y, Inaba K (2015) Geochemistry of two shallow CO2 seeps in Shikine Island (Japan) and their potential for ocean acidification research. Reg Stud Mar Sci 2:45–53. https://doi.org/10.1016/j.rsma.2015.07.004
Agostini S, Harvey BP, Wada S, Kon K, Milazzo M, Inaba K, Hall-Spencer JM (2018) Ocean acidification drives community shifts towards simplified non-calcified habitats in a subtropical − temperate transition zone. Sci Rep 8:11354. https://doi.org/10.1038/s41598-018-29251-7
Allen R, Foggo A, Fabricius K, Balistreri A, Hall-Spencer JM (2017) Tropical CO2 seeps reveal the impact of ocean acidification on coral reef invertebrate recruitment. Mar Pollut Bull 124:607–613. https://doi.org/10.1016/j.marpolbul.2016.12.031
Arima H (2014) ヤドカリ. SEIBUNDO SHINKOSHA, Japan
Briffa M, de la Haye K, Munday PL (2012a) High CO2 and marine animal behaviour: potential mechanisms and ecological consequences. Mar Pollut Bull 64:1519–1528. https://doi.org/10.1016/j.marpolbul.2012.05.032
Briffa M, de la Haye K, Munday PL (2012b) High CO2 and marine animal behaviour: potential mechanisms and ecological consequences. Mar Pollut Bull 64:1519–1528. https://doi.org/10.1016/j.marpolbul.2012.05.032
Broecker WS, Peng T-H (1974) Gas exchange rates between air and sea. Tellus 26:611. https://doi.org/10.3402/tellusa.v26i5.9869
Cigliano M, Gambi MC, Rodolfo-Metalpa R, Patti FP, Hall-Spencer JM (2010) Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents. Mar Biol 157:2489–2502. https://doi.org/10.1007/s00227-010-1513-6
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143
Clements J, Hunt H (2015) Marine animal behaviour in a high CO2 ocean. Mar Ecol Prog Ser 536:259–279. https://doi.org/10.3354/meps11426
Dore JE, Lukas R, Sadler DW, Church MJ, Karl DM (2009) Physical and biogeochemical modulation of ocean acidification in the central North Pacific. PNAS 106:12235–12240. https://doi.org/10.1073/pnas.0906044106
Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Change 1:165–169. https://doi.org/10.1038/nclimate1122
Fabricius KE, De’ath G, Noonan S, Uthicke S (2013) Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities. J Exp Mar Biol Ecol 24:0–7
Garilli V, Rodolfo-Metalpa R, Scuderi D, Brusca L, Parrinello D, Rastrick SPSS, Foggo A, Twitchett RJ, Hall-Spencer JM, Milazzo M (2015) Physiological advantages of dwarfing in surviving extinctions in high-CO2 oceans. Nat Clim Change 5:678–682. https://doi.org/10.1038/nclimate2616
Garrard SL, Gambi MC, Scipione MB, Patti FP, Lorenti M, Zupo V, Paterson DM, Buia MC (2014) Indirect effects may buffer negative responses of seagrass invertebrate communities to ocean acidification. J Exp Mar Biol Ecol 461:31–38. https://doi.org/10.1016/j.jembe.2014.07.011
Glandon HL, Kilbourne KH, Schijf J, Miller TJ (2018) Counteractive effects of increased temperature and pCO2on the thickness and chemistry of the carapace of juvenile blue crab, Callinectes sapidus, from the Patuxent River, Chesapeake Bay. J Exp Mar Biol Ecol 498:39–45. https://doi.org/10.1016/j.jembe.2017.11.005
Hall-Spencer JM, Allen R (2015) The impact of CO2 emissions on “nuisance” marine species. Res Rep Biodivers Stud 4:33–46. https://doi.org/10.2147/RRBS.S70357
Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia M-C (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99. https://doi.org/10.1038/nature07051
Hamasaki K, Hatta S, Ishikawa T, Yamashita S, Dan S, Kitada S (2015) Emigration behavior and molting during the sea-to-land transition of terrestrial hermit crabs under laboratory conditions. Invertebr Biol 134:318–331. https://doi.org/10.1111/ivb.12107
Harvey AW, Colasurdo EA (1993) Effects of shell and food availability on metamorphosis in the hermit crabs Pagurus hirsutiusculus (Dana) and Pagurus granosimanus (Stimpson). J Exp Mar Biol Ecol 165:13
Harvey BP, McKeown NJ, Rastrick SPS, Bertolini C, Foggo A, Graham H, Hall-Spencer JM, Milazzo M, Shaw PW, Small DP, Moore PJ (2016) Individual and population-level responses to ocean acidification. Scientific Reports 6:20194. https://doi.org/10.1038/srep20194
Hasegawa H, Wada S, Aoki M, Wada K (2009) Regional variation in shell utilization patterns of the hermit crab Pagurus filholi. Plankton Benthos Res 4:72–76. https://doi.org/10.3800/pbr.4.72
Hasegawa H, Wada S, Aoki M, Wada K (2011) Regional variation in preference for gastropod shell species in the hermit crab Pagurus filholi. J Mar Biol Assoc UK 91:893–896. https://doi.org/10.1017/S0025315410000561
Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Gr Stat 5:299–314
Imazu M, Asakura A (1994) Distribution, reproduction and shell utilization patterns in 3 species of intertidal hermit-crabs on a rocky shore on the pacific coast of Japan. J Exp Mar Biol Ecol 184:41–65. https://doi.org/10.1016/0022-0981(94)90165-1
IPCC (2015) Climate change 2014: synthesis report. Intergovernmental Panel on Climate Change. IPCC, Geneva
Ishii M, Kosugi N, Sasano D, Saito S, Midorikawa T, Inoue HY (2011) Ocean acidification off the south coast of Japan: a result from time series observations of CO2 parameters from 1994 to 2008. J Geophys Res 116:1–9. https://doi.org/10.1029/2010JC006831
Jutfelt F, Bresolin de Souza K, Vuylsteke A, Sturve J (2013) Behavioural disturbances in a temperate fish exposed to sustained high-CO2 levels. PLoS ONE 8:6–11. https://doi.org/10.1371/journal.pone.0065825
Kornienko ES, Korn OM (2016) A key for the identification of the zoeae of common species of hermit crabs (Decapoda: Paguroidea) of Vostok Bay, the Sea of Japan. Russ J Mar Biol 42:419–426. https://doi.org/10.1134/S1063074016050047
Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso JP (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Change Biol 19:1884–1896. https://doi.org/10.1111/gcb.12179
Leduc AOHC, Munday PL, Brown GE, Ferrari MCO (2013) Effects of acidification on olfactory-mediated behaviour in freshwater and marine ecosystems: a synthesis. Philos Trans R Soc B Biol Sci 368:20120447. https://doi.org/10.1098/rstb.2012.0447
Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations, ORNL/CDIAC-105. Carbon Dioxide Inf Anal Cent, Oak Ridge Natl Lab, Oak Ridge, Tenn 38
Okutani T (2017) Marine mollusks in Japan, 2nd edn. Tokai University Press, Japan
Passarelli MC, Cesar A, Riba I, DelValls TA (2017) Comparative evaluation of sea-urchin larval stage sensitivity to ocean acidification. Chemosphere 184:224–234. https://doi.org/10.1016/j.chemosphere.2017.06.001
Rodolfo-Metalpa R, Houlbrèque F, Tambutté É, Boisson F, Baggini C, Patti FP, Jeffree R, Fine M, Foggo A, Gattuso J-P, Hall-Spencer JM (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nat Clim Change 1:308–312. https://doi.org/10.1038/nclimate1200
Roy RN, Roy LN, Vogel KM, Portermoore C, Pearson T, Good CE, Millero FJ, Campbell DM (1993) The dissociation-constants of carbonic-acid in seawater at salinities 5 to 45 and temperatures 0 to 45 °C. Mar Chem 44:249–267. https://doi.org/10.1016/0304-4203(93)90207-5
Scully EP (1979) The effects of gastropod shell availability and habitat characteristics on shell utilization by the intertidal hermit crab Pagurus longicarpus Say. J Exp Mar Biol Ecol 37:139–152. https://doi.org/10.1016/0022-0981(79)90091-1
Sheppard Brennand H, Soars N, Dworjanyn SA, Davis AR, Byrne M (2010) Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS ONE 5:1–7. https://doi.org/10.1371/journal.pone.0011372
Straughan NA, Gosselin LA (2014) Ontogenetic changes in shell preferences and resource partitioning by the hermit crabs Pagurus hirsutiusculus and P. granosimanus. J Exp Mar Biol Ecol 451:1–8. https://doi.org/10.1016/j.jembe.2013.10.028
Strauss S (1991) Indirect effects in community ecology: their definition, study and importance. Trends Ecol Evol 6:206–210. https://doi.org/10.1016/0169-5347(91)90023-Q
Turra A, Leite FPP (2007) Embryonic development and duration of incubation period of tropical intertidal hermit crabs (Decapoda, Anomura). Revista Brasileira de Zoologia 24:677–686. https://doi.org/10.1590/S0101-81752007000300020
Vernberg WB, DeCoursey PJ, Padgett WJ (1973) Synergistic effects of environmental variables on larvae of Uca pugilator. Mar Biol 22:307–312. https://doi.org/10.1007/BF00391386
Wada S, Tanaka K, Goshima S (1999) Precopulatory mate guarding in the hermit crab Pagurus middendorffii (Brandt) (Decapoda: Paguridae): effects of population parameters on male guarding duration. J Exp Mar Biol Ecol 239:289–298
Wada S, Mima A, Ito A (2005) Reproductive phenology of sympatric hermit crabs in temperate Japan. J Mar Biol Assoc UK 85:889–894. https://doi.org/10.1017/S0025315405011859
Walther K, Anger K, Pörtner H (2010) Effects of ocean acidification and warming on the larval development of the spider crab Hyas araneus from different latitudes (54° vs. 79°N). Mar Ecol Prog Ser 417:159–170. https://doi.org/10.3354/meps08807
Wittmann AC, Pörtner H-O (2013) Sensitivities of extant animal taxa to ocean acidification. Nat Clim Change 3:995–1001. https://doi.org/10.1038/nclimate1982
Yoshino K, Goshima S, Nakao S (1999) The interaction between shell size and shell species preferences of the hermit crab Pagurus filholi. Benthos research 54:37–44
Acknowledgements
The authors thank the technical staff of the Shimoda Marine Research Center, University of Tsukuba (Yasutaka Tsuchiya, Toshihiko Sato, Daisuke Shibata, Manabu Ooue, Tomomi Kodaka, and Jiro Takano) for their assistance during the experiments and specimen sampling. The first author received financial support from a Research Fellowship from the Japan Society for the Promotion of Science for Young Scientists. The present work was supported by grants-in-aid from the Japan Society for the Promotion of Science (Nos. 16J00443 and 18H02219). We would like to thank Editage (www.editage.jp) for English language editing.
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Tomatsuri, M., Kon, K. Impacts of ocean acidification on hermit crab communities through contrasting responses of Pagurus filholi (de Man, 1887) and Clibanarius virescens (Krauss, 1843). Aquat Ecol 53, 569–580 (2019). https://doi.org/10.1007/s10452-019-09709-0
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Keywords
- Ocean acidification
- Hermit crab
- Direct/indirect effect
- CO2 seep
- Environmental stress