Abstract
It is crucial to understand the role of temperature in rearing sea urchin larvae for large-scale production of sea urchin seeds. The development of purple sea urchins, Heliocidaris crassispina, such as fertilization, hatching, embryonic development, larval growth, ingestion, metabolism, and metamorphosis, was investigated at four temperatures: 20, 24, 28, and 32 °C. In the four temperatures, fertilization and hatching of sea urchins first increased with temperature and then decreased. The optimal condition was found at a temperature of 28 °C, where the fertilization and hatching rates exceeded 90%, and embryonic development was highly synchronized. This condition did not differ from the results observed at a temperature of 24 °C (P > 0.05). The fertilization and hatching rates were lower at 20 °C and 32 °C, among which 32 °C had the fastest embryo development but the second highest mortality. In contrast, 20 °C had the slowest embryo development and the most increased mortality. The optimal growth temperature for larvae is 28 °C, at which their growth and development rate are the fastest. However, at 24 °C, it is the second highest. At 20 °C, the growth rate is the lowest, with sluggish physiological responses and the lowest digestion and metabolism capacity. The metamorphosis rate did not differ between 28 and 32 °C (P < 0.05), with 50.0% and 61.1%, respectively, while remaining below 4% at 20 °C. This indicates that temperature significantly impacts the early development of Heliocidaris crassispina sea urchins, whose larvae may be sensitive to low temperatures but have higher temperature tolerance.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Data availability
All of the data and material is owned by the corresponding author.
References
Agatsuma Y (2013) Hemicentrotus pulcherrimus, Pseudocentrotus depressus, and Heliocidaris crassispina. In: Lawrence JM (ed) Sea urchins: biology and ecology, 3rd edn. Elsevier, Amsterdam, pp 461–473. https://doi.org/10.1016/B978-0-12-396491-5.00030-7
Allen JD (2008) Size-specific predation on marine invertebrate larvae. Biol Bull 214:42–49. https://doi.org/10.2307/25066658
Andronikov VB (1975) Heat resistance of gametes of marine invertebrates in relation to temperature conditions under which the species exist. Mar Biol 30:1–11. https://doi.org/10.1007/BF00393747
Anthony KRN, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R (2009) Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct Ecol 23:539–550. https://doi.org/10.1111/j.1365-2435.2008.01531.x
Artigaud S, Richard J, MaS T, Lavaud R, Flye-Sainte-Marie J, Jean F, Peck LS, Clark MS, Pichereau V (2015) Deciphering the molecular adaptation of the king scallop (Pecten maximus) to heat stress using transcriptomics and proteomics. BMC Genomics 16:988. https://doi.org/10.1186/s12864-015-2132-x
Bögner D (2016) Life under climate change scenarios: sea urchins’ cellular mechanisms for reproductive success. J Mar Sci Eng 4:28. https://doi.org/10.3390/jmse4010028
Bögner D, Bickmeyer U, Köhler A (2014) CO2-induced fertilization impairment in Strongylocentrotus droebachiensis collected in the Arctic. Helgol Mar Res 68:341–356. https://doi.org/10.1007/s10152-014-0394-3
Brierley AS, Kingsford MJ (2009) Impacts of climate change on marine organisms and ecosystems. Curr Biol 19:R602–R614. https://doi.org/10.1016/j.cub.2009.05.046
Buitrago E, Lodeiros C, Lunar K, Alvarado D, Indorf F, Frontado K, Moreno P, Vasquez Z (2005) Mass production of competent larvae of the sea urchin Lytechinus variegatus (Echinodermata: Echinoidea). Aquacult Int 13:359–367. https://doi.org/10.1007/s10499-004-6551-y
Byrne M, Ho M, Selvakumaraswamy P, Nguyen HD, Dworjanyn SA, Davis AR (2009) Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios. Proc R Soc B 276:1883–1888. https://doi.org/10.1098/rspb.2008.1935
Byrne M, Selvakumaraswamy P, Ho M, Woolsey E, Nguyen H (2011) Sea urchin development in a global change hotspot, potential for southerly migration of thermotolerant propagules. Deep Sea Res II 58:712–719. https://doi.org/10.1016/j.dsr2.2010.06.010
Byrne M, Ross PM, Dworjanyn SA, Parker L (2017) Larval ecology in the face of changing climate-impacts of ocean warming and ocean acidification. In: Carrier TJ, Reitzel AM, Heyland A (eds) Evolutionary ecology of marine invertebrate larvae. Oxford University Press, New York, pp 251–272. https://doi.org/10.1093/oso/9780198786962.003.0017
Cameron RA, Hinegardner RT (1974) Initiation of metamorphosis in laboratory cultured sea urchins. Biol Bull 146:335–342. https://doi.org/10.2307/1540409
Chiu ST (1984) Feeding biology of the short spined sea urchin Anthocidaris crassispina (A.Agassiz) in Hong Kong. In: Keegan B, O’connor B (eds) Echinodermata. CRC Press, Balkema Boston, pp 223–232. https://doi.org/10.1201/9781003079224-45
Clark AM (1982) Echinoderms of Hong Kong. In: Tseng C-K (ed) Proceedings of the first international marine biological workshop: the marine flora and fauna of Hong Kong and southern China. Hong Kong University Press, Hong Kong, pp 485–501
Diaz-Perez L, Carpizo-Ituarte E (2011) Effect of thermal stress on survival and delay of metamorphosis in larvae of the purple sea urchin Strongylocentrotus purpuratus. Cienc Mar 37:403–414. https://doi.org/10.7773/cm.v37i4A.1903
Ding J, Chang Y, Wang C, Cao X (2007) Evaluation of the growth and heterosis of hybrids among three commercially important sea urchins in China: Strongylocentrotus nudus, S-intermedius and Anthocidaris crassispina. Aquaculture 272:273–280. https://doi.org/10.1016/j.aquaculture.2007.07.231
Dworjanyn SA, Pirozzi I (2008) Induction of settlement in the sea urchin Tripneustes gratilla by macroalgae, biofilms and conspecifics: a role for bacteria? Aquaculture 274:268–274. https://doi.org/10.1016/j.aquaculture.2007.11.030
Eldridge WH, Sweeney BW, Law JM (2015) Fish growth, physiological stress, and tissue condition in response to rate of temperature change during cool or warm diel thermal cycles. Can J Fish AquatSci 72:1527–1537. https://doi.org/10.1139/cjfas-2014-0350
Emlet RB (1983) Locomotion, drag, and the rigid skeleton of larval echinoderms. Biol Bull 164:433–445
Farmanfarmaian A, Giese AC (1963) Thermal tolerance and acclimation in the western purple sea urchin, Strongylocentrotus purpuratus. Physiol Zool 36:237–243
Feng D, Ke C, Lu C, Li S (2010) The influence of temperature and light on larval pre-settlement metamorphosis: a study of the effects of environmental factors on pre-settlement metamorphosis of the solitary ascidian Styela canopus. Mar Freshwater Behav Physiol 43:11–24. https://doi.org/10.1080/10236240903523204
Feng W, Nakabayashi N, Narita K, Inomata E, Aoki MN, Agatsuma Y (2019) Reproduction and population structure of the sea urchin Heliocidaris crassispina in its newly extended range: the Oga Peninsula in the Sea of Japan, northeastern Japan. PLoS One 14:e0209858. https://doi.org/10.1371/journal.pone.0209858
Foo SA, Dworjanyn SA, Poore AGB, Byrne M (2012) Adaptive capacity of the habitat modifying sea urchin Centrostephanus rodgersii to ocean warming and ocean acidification: performance of early embryos. PLOS ONE 7(8):e42497. https://doi.org/10.1371/journal.pone.0042497
Freeman SM (2003) Size-dependent distribution, abundance and diurnal rhythmicity patterns in the short-spined sea urchin Anthocidaris crassispina. Estuar Coast Shelf Sci 58:703–713. https://doi.org/10.1016/s0272-7714(03)00134-3
Fujisawa H (1989) Differences in temperature dependence of early development of sea urchins with different growing seasons. Biol Bull 176:96–102
Fujisawa H, Shigei M (1990) Correlation of embryonic temperature sensitivity of sea-urchins with spawning season. J Exp Mar Biol Ecol 136:123–139. https://doi.org/10.1016/0022-0981(90)90191-e
Gosselin P, Jangoux M (1996) Induction of metamorphosis in Paracentrotus lividus larvae (Echinodermata, Echinoidea). Oceanolog Acta 19:293–296
Grosjean P, Spirlet C, Gosselin P, Vaitilingon D, Jangoux M (1998) Land-based, closed-cycle echiniculture of Paracentrotus lividus (Lamarck) (Echinoldea: Echinodermata): a long-term experiment at a pilot scale. J Shellfish Res 17:1523–1531
Grünbaum D, Strathmann RR (2003) Form, performance and trade-offs in swimming and stability of armed larvae. J Mar Res 61:659–691. https://doi.org/10.1357/002224003771815990
Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci USA 104:1745–1750. https://doi.org/10.1073/pnas.0610108104
Hardy NA, Byrne M (2014) Early development of congeneric sea urchins (Heliocidaris) with contrasting life history modes in a warming and high CO2 ocean. Mar Environ Res 102:78–87. https://doi.org/10.1016/j.marenvres.2014.07.007
Hernández JM, León-Santana M, León CJ (2007) The role of the water temperature in the optimal management of marine aquaculture. Eur J Oper Res 181:872–886. https://doi.org/10.1016/j.ejor.2006.06.021
Hoegh-Guldberg O, Pearse JS (1995) Temperature, food availability, and the development of marine invertebrate larvae. Am Zool 35:415–425. https://doi.org/10.1093/icb/35.4.415
Hoffmann KH (1983) Metabolic and enzyme adaptation to temperature and pressure. In: Hochachka PW (ed) The Mollusca. Academic Press, San Diego, pp 219–255. https://doi.org/10.1016/B978-0-12-751402-4.50013-3
Hoffmann AA, Sgro CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485. https://doi.org/10.1038/nature09670
Hofmann GE, Todgham AE (2010) Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annu Rev Physiol 72:127–145. https://doi.org/10.1146/annurev-physiol-021909-135900
Huggett MJ, Williamson JE, De Nys R, Kjelleberg S, Steinberg PD (2006) Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia 149:604–619. https://doi.org/10.1007/s00442-006-0470-8
IPCC (2014) Climate change 2014: synthesis report. In: Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, p 105
Kuo ESL, Sanford E (2009) Geographic variation in the upper thermal limits of an intertidal snail: implications for climate envelope models. Mar Ecol Prog Ser 388:137–146. https://doi.org/10.3354/meps08102
Lamare MD, Barker MF (1999) In situ estimates of larval development and mortality in the New Zealand sea urchin Evechinus chloroticus (Echinodermata: Echinoidea). Mar Ecol Prog Ser 180:197–211. https://doi.org/10.3354/meps180197
Lawrence JM (2013) Sea urchins: biology and ecology, 3rd edn. Elsevier, Amsterdam
Lawrence JM, Agatsuma Y (2007) Ecology of Tripneustes. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 499–520. https://doi.org/10.1016/S0167-9309(07)80088-3
Lawrence JM, Zhao C, Chang Y-Q (2019) Large-scale production of sea urchin (Strongylocentrotus intermedius) seed in a hatchery in China. Aquacult Int 27:1–7. https://doi.org/10.1007/s10499-018-0319-2
Liu H, Chang Y-Q (2015) Sea urchin aquaculture in China. In: Brown NP, Eddy SD (eds) Echinoderm aquaculture. Wiley, New York, pp 127–146. https://doi.org/10.1002/9781119005810.ch6
Lu XY, Wu RSS (2005) UV induces reactive oxygen species, damages sperm, and impairs fertilisation in the sea urchin Anthocidaris crassispina. Mar Biol 148:51–57. https://doi.org/10.1007/s00227-005-0049-7
Mak KK-Y, Chan KYK (2018) Interactive effects of temperature and salinity on early life stages of the sea urchin Heliocidaris crassispina. Mar Biol 165:1–11. https://doi.org/10.1007/s00227-018-3312-4
Maldonado M, Young CM (1996) Effects of physical factors on larval behavior, settlement and recruitment of four tropical demosponges. Mar Ecol Prog Ser 138:169–180. https://doi.org/10.3354/meps138169
Margarita Mejia-Gutierrez L, Benitez-Villalobos F, Patricia Diaz-Martinez J (2019) Effect of temperature increase on fertilization, embryonic development and larval survival of the sea urchin Toxopneustes roseus in the Mexican south Pacific. J Therm Biol 83:157–164. https://doi.org/10.1016/j.jtherbio.2019.05.011
Minuti JJ, Byrne M, Hemraj DA, Russell BD (2021) Capacity of an ecologically key urchin to recover from extreme events: physiological impacts of heatwaves and the road to recovery. Sci Total Environ 785:147281. https://doi.org/10.1016/j.scitotenv.2021.147281
Minuti JJ, Byrne M, Campbell H, Hemraj DA, Russell BD (2022) Live-fast-die-young: carryover effects of heatwave-exposed adult urchins on the development of the next generation. Global Change Biol 28:5781–5792. https://doi.org/10.1111/gcb.16339
Mos B, Cowden KL, Nielsen SJ, Dworjanyn SA (2011) Do cues matter? Highly inductive settlement cues don’t ensure high post-settlement survival in sea urchin aquaculture. PLoS ONE 6:e28054. https://doi.org/10.1371/journal.pone.0028054
Mueter FJ, Litzow MA (2008) Sea ice retreat alters the biogeography of the Bering Sea continental shelf. Ecol Appl 18:309–320. https://doi.org/10.1890/07-0564.1
O’connor C, Mulley J (1977) Temperature effects on periodicity and embryology, with observations on the population genetics, of the aquacultural echinoid Heliocidaris tuberculata. Aquaculture 12:99–114. https://doi.org/10.1016/0044-8486(77)90176-4
Palmer RA (1994) Temperature sensitivity, rate of development, and time to maturity: geographic variation in laboratory-reared Nucella and a cross-phyletic overview. In: Wilson WH, Stricker SA, Shinn GL (eds) Reproduction and development of marine invertebrates. Johns Hopkins University Press, Baltimore, pp 177–194
Pearce CM, Scheibling RE (1991) Effect of macroalgae, microbial films, and conspecifics on the induction of metamorphosis of the green sea-urchin Strongylocentrotus-droebachiensis (Muller). J Exp Mar Biol Ecol 147:147–162. https://doi.org/10.1016/0022-0981(91)90179-z
Pecorino D, Lamare MD, Barker MF, Byrne M (2013) How does embryonic and larval thermal tolerance contribute to the distribution of the sea urchin Centrostephanus rodgersii (Diadematidae) in New Zealand? J Exp Mar Biol Ecol 445:120–128. https://doi.org/10.1016/j.jembe.2013.04.013
Poloczanska ES, Babcock RC, Butler A, Hobday A, Hoegh-Guldberg O, Kunz TJ, Matear R, Milton DA, Okey TA, Richardson AJ (2007) Climate change and Australian marine life. Oceanogr Mar Biol 45:407–478. https://doi.org/10.1201/9781420050943.ch8
Pörtner HO (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol a: Mol Integr Physiol 132:739–761. https://doi.org/10.1016/S1095-6433(02)00045-4
Przeslawski R, Ahyong S, Byrne M, Wörheide G, Hutchings P (2008) Beyond corals and fish: the effects of climate change on noncoral benthic invertebrates of tropical reefs. Global Change Biol 14:2773–2795. https://doi.org/10.1111/j.1365-2486.2008.01693.x
Quiniou F, Guillou M, Judas A (1999) Arrest and delay in embryonic development in sea urchin populations of the Bay of Brest (Brittany, France): link with environmental factors. Mar Pollut Bull 38:401–406. https://doi.org/10.1016/S0025-326X(98)90159-X
Rahim S, Li JY, Kitamura H (2004) Larval metamorphosis of the sea urchins, Pseudocentrotus depressus and Anthocidaris crassispina in response to microbial films. Mar Biol 144:71–78. https://doi.org/10.1007/s00227-003-1171-z
Rahman S, Tsuchiya M, Uehara T (2009) Effects of temperature on hatching rate, embryonic development and early larval survival of the edible sea urchin, Tripneustes gratilla. Biologia 64:768–775. https://doi.org/10.2478/s11756-009-0135-2
Reitzel AM, Miner BG, Mcedward LR (2004) Relationships between spawning date and larval development time for benthic marine invertebrates: a modeling approach. Mar Ecol Prog Ser 280:13–23. https://doi.org/10.3354/meps280013
Roccheri MC, Sconzo G, Larosa M, Oliva D, Abrignani A, Giudice G (1986) Response to heat-shock of different sea-urchin species. Cell Differ 18:131–135. https://doi.org/10.1016/0045-6039(86)90007-2
Rupp JH (1973) Effects of temperature on fertilization and early cleavage of some tropical echinoderms, with emphasis on Echinometra mathaei. Mar Biol 23:183–189. https://doi.org/10.1007/BF00389483
Sanford E (2002) Water temperature, predation, and the neglected role of physiological rate effects in rocky intertidal communities. Integr Comp Biol 42:881–891. https://doi.org/10.1093/icb/42.4.881
Sarifudin M, Rahman MA, Yusoff FM, Arshad A, Tan SG (2016) Effects of temperature on the embryonic and early larval development in tropical species of black sea urchin, Diadema setosum (Leske, 1778). J Environ Biol 37:657–668
Schirone RC, Gross L (1968) Effect of temperature on early embryological development of the zebra fish, Brachydanio rerio. J Exp Zool 169:43–52. https://doi.org/10.1002/jez.1401690106
Sewell MA, Young CM (1999) Temperature limits to fertilization and early development in the tropical sea urchin Echinometra lucunter. J Exp Mar Biol Ecol 236:291–305. https://doi.org/10.1016/S0022-0981(98)00210-X
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:e11372. https://doi.org/10.1371/journal.pone.0011372
Shigai X, Chuanxin Q, Zhenhua M, Gang Y, Jinhui S, Wanni P, Tao Z, Hongmei M, Wentao Z (2020) Effects of dietary microalgae on growth and survival of larval development of sea urchin (Anthocidaris crassispina). South China Fish Sci 16:115–120
Shimabukuro S (1991) Tripneustes gratilla (sea urchin). In: Shokita SYM, Masashi M (eds) Aquaculture in tropical areas. Midori Shobo, Japan, Tokyo, pp 313–328
Sin E, Min WG, Kim Y-B, Kim TW (2019) Respiration of the sea urchin Mesocentrotus nudus in response to large temperature fluctuations. Mar Environ Res 144:178–185. https://doi.org/10.1016/j.marenvres.2019.01.003
Smith MM, Cruz Smith L, Cameron R, LA Andrew U (2008) The larval stages of the sea urchin, Strongylocentrotus purpuratus. J Morphol 269:713–733. https://doi.org/10.1002/jmor.10618
Soars NA, TaA P, Byrne M (2009) Overview of phenotypic plasticity in echinoid larvae, ‘Echinopluteus transversus’ type vs. typical echinoplutei. Mar Ecol Prog Ser 383:113–125. https://doi.org/10.3354/meps07848
Sokolova IM, Portner HO (2001) Temperature effects on key metabolic enzymes in Littorina saxatilis and L. obtusata from different latitudes and shore levels. Mar Biol 139:113–126. https://doi.org/10.1007/s002270100557
Sokolova IM, Portner HO (2003) Metabolic plasticity and critical temperatures for aerobic scope in a eurythermal marine invertebrate (Littorina saxatilis, Gastropoda: Littorinidae) from different latitudes. J Exp Biol 206:195–207. https://doi.org/10.1242/jeb.00054
Spanopoulos-Hernández M, Martínez-Palacios CA, Vanegas-Pérez RC, Rosas C, Ross LG (2005) The combined effects of salinity and temperature on the oxygen consumption of juvenile shrimps Litopenaeus stylirostris (Stimpson, 1874). Aquaculture 244:341–348. https://doi.org/10.1016/j.aquaculture.2004.11.023
Stanwell-Smith D, Peck LS (1998) Temperature and embryonic development in relation to spawning and field occurrence of larvae of three Antarctic echinoderms. Biol Bull 194:44–52. https://doi.org/10.2307/1542512
Stumpp M, Wren J, Melzner F, Thorndyke MC, Dupont ST (2011) CO2 induced seawater acidification impacts sea urchin larval development I: elevated metabolic rates decrease scope for growth and induce developmental delay. Comp Biochem Physiol a: Mol Integr Physiol 160:331–340. https://doi.org/10.1016/j.cbpa.2011.06.022
Thompson G (1982) Underwater observations on the distribution of regular sea urchins in Hong Kong. The marine flora and fauna of Hong Kong and Southern China. Hong Kong University Press, Hong Kong, pp 655–671
Tomanek L (2008) The importance of physiological limits in determining biogeographical range shifts due to global climate change: the heat-shock response. Physiol Biochem Zool 81:709–717. https://doi.org/10.1086/590163
Urriago JD, Wong JCY, Dumont CP, Qiu J-W (2016) Reproduction of the short-spined sea urchin Heliocidaris crassispina (Echinodermata: Echinoidea) in Hong Kong with a subtropical climate. Reg Stud Mar Sci 8:445–453. https://doi.org/10.1016/j.rsma.2016.03.005
Vaschenko MA, Zhang ZP, Lam PKS, Wu RSS (1999) Toxic effects of cadmium on fertilizing capability of spermatozoa, dynamics of the first cleavage and pluteus formation in the sea urchin Anthocidaris crassispina (Agassiz). Mar Pollut Bull 38:1097–1104. https://doi.org/10.1016/s0025-326x(99)00116-2
Vernberg FJ (1983) Respiratory Adaptations. Environ Adaptations 8:1–42
Wang R, Liu T-M, Shen M-H, Yang M-Q, Feng Q-Y, Tang X-M, Li X-M (2012) Spiculisporic acids B-D, three new γ-butenolide derivatives from a sea urchin-derived fungus Aspergillus sp. HDf2. Molecules 17:13175–13182. https://doi.org/10.3390/molecules171113175
Wangensteen OS, Dupont S, Casties I, Turon X, Palacin C (2013) Some like it hot: temperature and pH modulate larval development and settlement of the sea urchin Arbacia lixula. J Exp Mar Biol Ecol 449:304–311. https://doi.org/10.1016/j.jembe.2013.10.007
Whalan S, Ettinger-Epstein P, De Nys R (2008) The effect of temperature on larval pre-settlement duration and metamorphosis for the sponge, Rhopaloeides odorabile. Coral Reefs 27:783–786. https://doi.org/10.1007/s00338-008-0400-9
Yoo SK (1982) Growth and spawning of the sea urchin Anthocidaria crassispina (A. Agassiz). Korean Fish Soc 15:345–358
Zhao C, Zhang L, Shi D, Ding J, Yin D, Sun J, Zhang B, Zhang L, Chang Y (2018) Transgenerational effects of ocean warming on the sea urchin Strongylocentrotus intermedius. Ecotoxicol Environ Saf 151:212–219. https://doi.org/10.1016/j.ecoenv.2018.01.014
Funding
The work was supported by the Special Project on the Science Foundation of Fujian Province (2021J01826), the Special Project on Blue Granary Science and Technology Innovation under the National Key R&D Program (grant number 2018YFD0901605), and the Youth Project (23YYST076QCB30)-Xiamen Municipal Ocean Development Bureau, Fujian Province.
Author information
Authors and Affiliations
Contributions
JY: validation, formal analysis, writing—original draft. LZ: conceptualization, project administration. SH: resources, supervision. GW: conceptualization, methodology, funding acquisition, writing—review and editing.
Corresponding author
Ethics declarations
Ethics approval
The manuscript is conducted within the ethical manner advised by the targeted journal.
Competing interests
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Handling Editor: Gavin Burnell
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yu, J., Wang, G., Zhang, L. et al. Effects of temperature on fertilization, hatching, larval growth, ingestion, metabolism, and metamorphosis of the purple sea urchins, Heliocidaris crassispina. Aquacult Int 32, 4597–4617 (2024). https://doi.org/10.1007/s10499-024-01392-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-024-01392-9