Physiological performance of three calcifying green macroalgae <i>Halimeda</i> species in response to altered seawater temperatures

Zhangliang Wei; Jiahao Mo; Ruiping Huang; Qunju Hu; Chao Long; Dewen Ding; Fangfang Yang; Lijuan Long

doi:10.1007/s13131-019-1471-3

Volume 39 Issue 2

Turn off MathJax

Article Contents

Article Navigation > Acta Oceanologica Sinica > 2020 > 39(2): 89-100

Zhangliang Wei, Jiahao Mo, Ruiping Huang, Qunju Hu, Chao Long, Dewen Ding, Fangfang Yang, Lijuan Long. Physiological performance of three calcifying green macroalgae Halimeda species in response to altered seawater temperatures[J]. Acta Oceanologica Sinica, 2020, 39(2): 89-100. doi: 10.1007/s13131-019-1471-3

Citation:

Zhangliang Wei, Jiahao Mo, Ruiping Huang, Qunju Hu, Chao Long, Dewen Ding, Fangfang Yang, Lijuan Long. Physiological performance of three calcifying green macroalgae Halimeda species in response to altered seawater temperatures[J]. Acta Oceanologica Sinica, 2020, 39(2): 89-100. doi: 10.1007/s13131-019-1471-3

Citation:

PDF( 1033 KB)

Physiological performance of three calcifying green macroalgae Halimeda species in response to altered seawater temperatures

doi: 10.1007/s13131-019-1471-3

Zhangliang Wei^{1, 2},
Jiahao Mo^{1, 2},
Ruiping Huang³,
Qunju Hu^{1, 2},
Chao Long^{1, 2},
Dewen Ding^{1, 4},
Fangfang Yang^{1
,
,},
Lijuan Long^{1
,
,}

1.
CAS Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
2.
University of Chinese Academy of Sciences, Beijing 100049, China
3.
State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen 361102, China
4.
First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China

Funds: The Guangzhou Science and Technology Project under contract No. 201707010174; the Strategic Priority Research Program of the Chinese Academy Sciences under contract No. XDA13020203; the Ocean Public Welfare Scientific Research Project under contract No. 201305018-3.

More Information

Corresponding author: E-mail: ycuyang@163.com; longlj@scsio.ac.cn
Received Date: 2018-12-20
Accepted Date: 2019-03-18

Available Online: 2020-04-21

Publish Date: 2020-02-25

Abstract

Abstract

The effects of seawater temperature on the physiological performance of three Halimeda species were studied for a period of 28 d. Five treatments were established for Halimeda cylindracea, Halimeda opuntia and Halimeda lacunalis, in triplicate aquaria representing a factorial temperature with 24°C, 28°C, 32°C, 34°C and 36°C, respectively. The average F_v/F_m of these species ranged from 0.732 to 0.756 between 24°C and 32°C but declined sharply between 34°C (0.457±0.035) and 36°C (0.122±0.014). Calcification was highest at 28°C, with net calcification rates (G_net) of (20.082±2.482) mg/(g·d), (12.825±1.623) mg/(g·d) and (6.411±1.029) mg/(g·d) for H. cylindracea, H. opuntia and H. lacunalis, respectively. Between 24°C and 32°C, the specific growth rate (SGR) of H. lacunalis (0.079%–0.110% d^–1) was lower than that of H. cylindracea (0.652%–1.644% d^–1) and H. opuntia (0.360%–1.527% d^–1). Three Halimeda species gradually bleached at 36°C during the study period. Malondialdehyde (MDA) and proline levels in tissues of the three Halimeda were higher in 34–36°C than those in 24–32°C. The results indicate that seawater temperature with range of 24–32°C could benefit the growth and calcification of these Halimeda species, however, extreme temperatures above 34°C have negative impacts. The measured physiological parameters also revealed that H. cylindracea and H. opuntia displayed broader temperature tolerance than H. lacunalis.
- calcifying macroalgae,
- climate change,
- seawater temperature,
- physiological performance,
- photosynthesis,
- calcification

FullText(HTML)

References(64)

References

[1]	Agegian C R. 1985. The biogeochemical ecology of Porolithon gardineri (Foslie). Honolulu: University of Hawaii, 178
[2]	Anderson B C. 2006. Response of tropical marine macroalgae to thermal stress [dissertation]. Boca Raton, FL: Florida Atlantic University
[3]	Beach K, Walters L, Vroom P, et al. 2003. Variability in the ecophysiology of Halimeda spp. (Chlorophyta, Bryopsidales) on Conch Reef, Florida Keys, USA. Journal of Phycology, 39(4): 633–643. doi: 10.1046/j.1529-8817.2003.02147.x
[4]	Bertucci A, Moya A, Tambutté S, et al. 2013. Carbonic anhydrases in anthozoan coralsja review. Bioorganic & Medicinal Chemistry, 21(6): 1437–1450
[5]	Biber P D, Irlandi E A. 2006. Temporal and spatial dynamics of macroalgal communities along an anthropogenic salinity gradient in Biscayne Bay (Florida, USA). Aquatic Botany, 85(1): 65–77. doi: 10.1016/j.aquabot.2006.02.002
[6]	Campbell J E, Fisch J, Langdon C, et al. 2016. Increased temperature mitigates the effects of ocean acidification in calcified green algae (Halimeda spp.). Coral Reefs, 35(1): 357–368. doi: 10.1007/s00338-015-1377-9
[7]	Castillo K D, Ries J B, Bruno J F, et al. 2014. The reef-building coral Siderastrea siderea exhibits parabolic responses to ocean acidification and warming. Proceedings of the Royal Society B: Biological Sciences, 281(1797): 20141856. doi: 10.1098/rspb.2014.1856
[8]	Collins M, Knutti R, Arblaster J, et al. 2013. Long-term climate change: projections, commitments and irreversibility. In: Stocker T F, Qin D, Plattner G K, et al., eds. Climate Change 2013: the Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press
[9]	Deser C, Phillips A S, Alexander M A. 2010. Twentieth century tropical sea surface temperature trends revisited. Geophysical Research Letters, 37(10): L10701
[10]	Dijoux L, Verbruggen H, Mattio L, et al. 2012. Diversity of Halimeda (Bryopsidales, Chlorophyta) in New Caledonia: a combined morphological and molecular study. Journal of Phycology, 48(6): 1465–1481. doi: 10.1111/jpy.12002
[11]	Edmunds P J, Brown D, Moriarty V. 2012. Interactive effects of ocean acidification and temperature on two scleractinian corals from Moorea, French Polynesia. Global Change Biology, 18(7): 2173–2183. doi: 10.1111/j.1365-2486.2012.02695.x
[12]	Famà P, Wysor B, Kooistra W H C F, et al. 2002. Molecular phylogeny of the genus Caulerpa (Caulerpales, Chlorophyta) inferred from chloroplast tufA gene. Journal of Phycology, 38(5): 1040–1050. doi: 10.1046/j.1529-8817.2002.t01-1-01237.x
[13]	Hall T A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41: 95–98
[14]	Hensley N M, Elmasri O L, Slaughter E I, et al. 2013. Two species of Halimeda, a calcifying genus of tropical macroalgae, are robust to epiphytism by cyanobacteria. Aquatic Ecology, 47(4): 433–440. doi: 10.1007/s10452-013-9456-x
[15]	Hillis-Colinvaux L. 1980. Ecology and taxonomy of Halimeda: primary producer of coral reefs. Advances in Marine Biology, 17: 1–327. doi: 10.1016/S0065-2881(08)60303-X
[16]	Hodges D M, DeLong J M, Forney C F, et al. 1999. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta, 207(4): 604–611. doi: 10.1007/s004250050524
[17]	Hoegh-Guldberg O, Mumby P J, Hooten A J, et al. 2007. Coral reefs under rapid climate change and ocean acidification. Science, 318(5857): 1737–1742. doi: 10.1126/science.1152509
[18]	Hofmann L C, Bischof K, Baggini C, et al. 2015. CO₂ and inorganic nutrient enrichment affect the performance of a calcifying green alga and its noncalcifying epiphyte. Oecologia, 177(4): 1157–1169. doi: 10.1007/s00442-015-3242-5
[19]	Hofmann L C, Heiden J, Bischof K, et al. 2014. Nutrient availability affects the response of the calcifying chlorophyte Halimeda opuntia (L.) J.V. Lamouroux to low pH. Planta, 239(1): 231–242. doi: 10.1007/s00425-013-1982-1
[20]	Hughes T P, Baird A H, Bellwood D R, et al. 2003. Climate change, human impacts, and the resilience of coral reefs. Science, 301(5635): 929–933. doi: 10.1126/science.1085046
[21]	Hurd C L, Hepburn C D, Currie K I, et al. 2009. Testing the effects of ocean acidification on algal metabolism: considerations for experimental designs. Journal of Phycology, 45(6): 1236–1251. doi: 10.1111/j.1529-8817.2009.00768.x
[22]	Jokiel P L, Maragos J E, Franzisket L. 1978. Coral growth: buoyant weight technique. In: Stoddart D R, Johannes R E, eds. Coral Reefs: Research Methods. Paris: UNESCO, 529–541
[23]	Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16(2): 111–120. doi: 10.1007/BF01731581
[24]	Kleypas J A, Feely R A, Fabry V J, et al. 2006. Impacts of ocean acidification on coral reefs and other marine calcifiers: a guide for future research. St. Petersburg, FL: NSF, NOAA, U.S. Geological Survey
[25]	Koch M, Bowes G, Ross C, et al. 2013. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology, 19(1): 103–132. doi: 10.1111/j.1365-2486.2012.02791.x
[26]	Kojima R, Hanyuda T, Kawai H. 2015. Taxonomic re-examination of Japanese Halimeda species using genetic markers, and proposal of a new species Halimeda ryukyuensis (Bryopsidales, Chlorophyta). Phycological Research, 63(3): 178–188. doi: 10.1111/pre.12095
[27]	Langdon C, Gattuso J P, Andersson A. 2010. Measurements of calcification and dissolution of benthic organisms and communities. In: Riebesell U, Fabry V J, Hansson L, et al., eds. Guide to Best Practices for Ocean Acidification Research and Data Reporting. Luxembourg: European Union, 213–232
[28]	Lee T C, Hsu B D. 2009. Disintegration of the cells of siphonous green alga Codium edule (Bryopsidales, Chlorophyta) under mild heat stress. Journal of Phycology, 45(2): 348–356. doi: 10.1111/j.1529-8817.2009.00656.x
[29]	Lis J T. 1980. Fractionation of DNA fragments by polyethylene glycol induced precipitation. Methods in Enzymology, 65: 347–353. doi: 10.1016/S0076-6879(80)65044-7
[30]	Littler M M, Littler D S, Hanisak M D. 1991. Deep-water rhodolith distribution, productivity, and growth history at sites of formation and subsequent degradation. Journal of Experimental Marine Biology and Ecology, 150(2): 163–182. doi: 10.1016/0022-0981(91)90066-6
[31]	Lough J M, Barnes D J. 2000. Environmental controls on growth of the massive coral Porites. Journal of Experimental Marine Biology and Ecology, 245(2): 225–243. doi: 10.1016/S0022-0981(99)00168-9
[32]	Manzello D P. 2010. Coral growth with thermal stress and ocean acidification: lessons from the eastern tropical Pacific. Coral Reefs, 29(3): 749–758. doi: 10.1007/s00338-010-0623-4
[33]	Martin S, Castets M D, Clavier J. 2006. Primary production, respiration and calcification of the temperate free-living coralline alga Lithothamnion corallioides. Aquatic Botany, 85(2): 121–128. doi: 10.1016/j.aquabot.2006.02.005
[34]	Martin S, Clavier J, Chauvaud L, et al. 2007. Community metabolism in temperate maerl beds. I. Carbon and carbonate fluxes. Marine Ecology Progress Series, 335: 19–29. doi: 10.3354/meps335019
[35]	Martin S, Gattuso J P. 2009. Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Global Change Biology, 15(8): 2089–2100. doi: 10.1111/j.1365-2486.2009.01874.x
[36]	McCulloch M, Falter J, Trotter J, et al. 2012. Coral resilience to ocean acidification and global warming through pH up-regulation. Nature Climate Change, 2(8): 623–627. doi: 10.1038/nclimate1473
[37]	McKenzie L J, Campbell S J. 2004. Surviving the summer heat: seagrass burns as corals bleach. Seagrass-Watch News, 19: 1
[38]	Millero F J. 2007. The marine inorganic carbon cycle. Chemical Reviews, 107(2): 308–341. doi: 10.1021/cr0503557
[39]	Millero F J, Graham T B, Huang Fen, et al. 2006. Dissociation constants of carbonic acid in seawater as a function of salinity and temperature. Marine Chemistry, 100(1–2): 80–94. doi: 10.1016/j.marchem.2005.12.001
[40]	Morton B, Blackmore G. 2001. South China Sea. Marine Pollution Bulletin, 42(12): 1236–1263. doi: 10.1016/S0025-326X(01)00240-5
[41]	Muehllehner N, Edmunds P J. 2008. Effects of ocean acidification and increased temperature on skeletal growth of two scleractinian corals, Pocillopora meandrina and Porites rus. In: Proceedings of the 11th International Coral Reef Symposium. Ft. Lauderdale, Florida: ICRS, 57–61
[42]	Nelson W A. 2009. Calcified macroalgae-critical to coastal ecosystems and vulnerable to change: a review. Marine and Freshwater Research, 60(8): 787–801. doi: 10.1071/MF08335
[43]	Payri C E. 1988. Halimeda contribution to organic and inorganic production in a Tahitian reef system. Coral Reefs, 6(3–4): 251–262. doi: 10.1007/BF00302021
[44]	Peach K E, Koch M S, Blackwelder P L, et al. 2017. Calcification and photophysiology responses to elevated pCO₂ in six Halimeda species from contrasting irradiance environments on Little Cayman Island reefs. Journal of Experimental Marine Biology and Ecology, 486: 114–126. doi: 10.1016/j.jembe.2016.09.008
[45]	Pierrot D, Lewis E, Wallace D W R. 2006. MS excel program developed for CO₂ system calculations. ORNL/CDIAC-105a, Oak Ridge, Tennessee: Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy
[46]	Potin P, Floc’h J Y, Augris C, et al. 1990. Annual growth rate of the calcareous red alga Lithothamnion corallioides (Corallinales, Rhodophyta) in the Bay of Brest, France. Hydrobiologia, 204(1): 263–267
[47]	Price N N, Hamilton S L, Tootell J S, et al. 2011. Species-specific consequences of ocean acidification for the calcareous tropical green algae Halimeda. Marine Ecology Progress Series, 440: 67–78. doi: 10.3354/meps09309
[48]	Reynaud S, Leclercq N, Romaine-Lioud S, et al. 2003. Interacting effects of CO₂ partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Global Change Biology, 9(11): 1660–1668. doi: 10.1046/j.1365-2486.2003.00678.x
[49]	Saunders G W, Kucera H. 2010. An evaluation of rbcL, tufA, UPA, LSU and ITS as DNA barcode markers for the marine green macroalgae. Cryptogamie Algologie, 31(4): 487–528
[50]	Shan Dapeng, Huang Jinguang, Yang Yutao, et al. 2007. Cotton GhDREB1 increases plant tolerance to low temperature and is negatively regulated by gibberellic acid. New Phytologist, 176(1): 70–81. doi: 10.1111/j.1469-8137.2007.02160.x
[51]	Sinutok S, Hill R, Doblin M A, et al. 2011. Warmer more acidic conditions cause decreased productivity and calcification in subtropical coral reef sediment-dwelling calcifiers. Limnology and Oceanography, 56(4): 1200–1212. doi: 10.4319/lo.2011.56.4.1200
[52]	Sun Yanguo, Wang Bo, Jin Shanghui, et al. 2013. Ectopic expression of arabidopsis glycosyltransferase UGT85A5 enhances salt stress tolerance in tobacco. PLoS One, 8(3): e59924. doi: 10.1371/journal.pone.0059924
[53]	Tamura K, Dudley J, Nei M, et al. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24(8): 1596–1599. doi: 10.1093/molbev/msm092
[54]	Teichberg M, Fricke A, Bischof K. 2013. Increased physiological performance of the calcifying green macroalga Halimeda opuntia in response to experimental nutrient enrichment on a Caribbean coral reef. Aquatic Botany, 104: 25–33. doi: 10.1016/j.aquabot.2012.09.010
[55]	Teichberg M, Martinetto P, Fox S E. 2012. Bottom-up versus top-down control of macroalgal blooms. In: Wiencke C, Bischof K, eds. Seaweed Biology. Berlin, Heidelberg: Springer, 449–467
[56]	Thorhaug A. 1976. Tropical macroalgae as pollution indicator organisms. Micronesica, 12(1): 49–68
[57]	Verbruggen H, De Clerck O, N’Yeurt A D R, et al. 2006. Phylogeny and taxonomy of Halimeda incrassata, including descriptions of H. kanaloana and H. heteromorpha spp. nov. (Bryopsidales, Chlorophyta). European Journal of Phycology, 41: 337–362. doi: 10.1080/09670260600709315
[58]	Verbruggen H, Littler D S, Littler M M. 2007. Halimeda pygmaea and Halimeda pumila (Bryopsidales, Chlorophyta): two new dwarf species from fore reef slopes in Fiji and the Bahamas. Phycologia, 46(5): 513–520. doi: 10.2216/07-01.1
[59]	Vogel N, Meyer F W, Wild C, et al. 2015. Decreased light availability can amplify negative impacts of ocean acidification on calcifying coral reef organisms. Marine Ecology Progress Series, 521: 49–61. doi: 10.3354/meps11088
[60]	Walters L J, Smith C M, Coyer J A, et al. 2002. Asexual propagation in the coral reef macroalga Halimeda (Chlorophyta, Bryopsidales): production, dispersal and attachment of small fragments. Journal of Experimental Marine Biology and Ecology, 278(1): 47–65. doi: 10.1016/S0022-0981(02)00335-0
[61]	Wellburn A R. 1994. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology, 144: 307–313. doi: 10.1016/S0176-1617(11)81192-2
[62]	Wernberg T, Russell B D, Thomsen M S, et al. 2011. Seaweed communities in retreat from ocean warming. Current Biology, 21(21): 1828–1832. doi: 10.1016/j.cub.2011.09.028
[63]	Wizemann A, Meyer F W, Hofmann C L, et al. 2015. Ocean acidification alters the calcareous microstructure of the green macro-alga Halimeda opuntia. Coral Reefs, 34(3): 941–954. doi: 10.1007/s00338-015-1288-9
[64]	Wizemann A, Meyer F W, Westphal H. 2014. A new model for the calcification of the green macro-alga Halimeda opuntia (Lamouroux). Coral Reefs, 33(4): 951–964. doi: 10.1007/s00338-014-1183-9