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Marine Biology

, 167:13 | Cite as

Vertical distribution of echinoid larvae in pH stratified water columns

  • Elizaldy A. MabolocEmail author
  • Grant Batzel
  • Daniel Grünbaum
  • Kit Yu Karen Chan
Short Note

Abstract

The abundance and distribution of many benthic marine organisms are shaped by the success of their dispersive larval life-history stage. An increasing number of studies have shown that ocean acidification negatively impacts the larval life-history stage, including those of echinoids which are commercially and ecologically important. However, little is known about the behavioral responses of echinoid larvae to different pH levels in the water column. Changes in vertical movement in response to the naturally occurring pH variations caused by biological activities and/or physical conditions could affect dispersal and recruitment. In this study, we quantified the vertical distribution of larval sand dollars, Dendraster excentricus (Echinodermata), in water columns with stratified layers of seawater varying in salinity and pH. When larval sand dollars swimming upwards in ambient seawater (pHNBS 7.86 ± 0.04) encountered a layer of low pH (pHNBS 7.54 ± 0.04) seawater, about half of the individuals (53 ± 28%) were aggregated near the transition layer 60 min after the start of the experiment. Preliminary video analysis showed larvae reversed their direction of travel and altered the shape of their helical swimming trajectories, upon encountering the transition layer moving from ambient to low pH water. In contrast, when larval sand dollars swimming upwards in acidified seawater encountered ambient seawater, they continued to swim upward to aggregate near the top of the column. In control water columns with uniform pH, larvae did not change swimming behavior regardless of whether pH was ambient or acidified and whether salinity was uniform or stratified. These results indicate that stratification itself did not strongly affect the vertical distributions of larvae. These observations suggest that echinoid larvae, and perhaps many other types of planktonic larvae, may use behavioral plasticity to reduce exposure to stresses from ocean acidification. The presence and effectiveness of these responses may improve the ability of larvae to cope with stressful, dynamic habitats, and hence may be significant to prediction of potential impacts of global climate change.

Notes

Acknowledgements

The authors would like to thank Richard Emlet and Sasha Seroy for their advice, and Rebecca Guenther from the Ocean Acidification Environmental Laboratory for her assistance. Daniel Tong helped in Fig. 1 preparation. This project was part of a 5-week Larval Biology Course at Friday Harbor Laboratories that took place during July–August 2016.

Funding

EAM was supported by the Hong Kong PhD Fellowship Scheme grant and The Charles Lambert Memorial Endowment, and a Research Grant Council Project [Project#: 26102515] to KC. DG gratefully acknowledges the support of NSF (OCE-1657992) and NOAA Washington Sea Grant (NA10OAR-4170057).

Compliance with ethical standards

Conflict of interest

All authors declare no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

227_2019_3629_MOESM1_ESM.pdf (351 kb)
Supplementary material 1 (PDF 351 kb)

References

  1. Allen RM, Metaxas A, Snelgrove PVR (2018) Applying movement ecology to marine animals with complex lifecycles. Annu Rev Mar Sci 10:19–42CrossRefGoogle Scholar
  2. Arellano SM, Reitzel AM, Button CA (2012) Variation in vertical distribution of sand dollar larvae relative to haloclines, food, and fish cues. J Exp Mar Biol Ecol 414:28–37CrossRefGoogle Scholar
  3. Boyd PW, Cornwall CE, Davidson A, Doney SC, Fourquez M, Hurd CL, Lima ID, Mcminn A (2016) Biological responses to environmental heterogeneity under future ocean conditions. Glob Change Biol 22:2633–2650CrossRefGoogle Scholar
  4. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365PubMedCrossRefPubMedCentralGoogle Scholar
  5. Chan KYK, Grünbaum D (2010) Temperature and diet modified swimming behaviors of larval sand dollar. Mar Ecol Prog Ser 415:45–59CrossRefGoogle Scholar
  6. Chan KYK, Grünbaum D, O’Donnell J (2011) Effects of ocean-acidification-induced morphological changes on larval swimming and feeding. J Exp Biol 214:3857–3867PubMedCrossRefPubMedCentralGoogle Scholar
  7. Chan KYK, Sewell MA, Byrne M (2018) Revisiting the larval dispersal black box in the Anthropocene. ICES J Mar Sci 75:1841–1848CrossRefGoogle Scholar
  8. Chia F-S, Buckland-Nicks J, Young CM (1984) Locomotion of marine invertebrate: a review. Can J Zool 62:1205–1222CrossRefGoogle Scholar
  9. Clay TW, Grünbaum D (2011) Swimming performance as a constraint on larval morphology in plutei. Mar Ecol Prog Ser 423:185–196CrossRefGoogle Scholar
  10. Clements JC, Bishop MM, Hunt HL (2017) Elevated temperature has adverse effects on GABA-mediated avoidance behaviour to sediment acidification in a wide-ranging marine bivalve. Mar Biol 164:56CrossRefGoogle Scholar
  11. Cyronak T, Anderson AJ, D’Angelo S, Bresnahan P, Davidson C, Griffin A, Kindeberg T, Pennise J, Takeshita Y, White M (2018) Short-term spatial and temporal carbonate chemistry variability in two contrasting seagrass meadows: implications for pH buffering capacities. Estuaries Coasts 41:1282–1296CrossRefGoogle Scholar
  12. Daigle RM, Metaxas A (2011) Vertical distribution of marine invertebrate larvae in response to thermal stratification in the laboratory. J Exp Mar Biol Ecol 409:89–98CrossRefGoogle Scholar
  13. Dekshenieks MM, Donaghay PL, Sullivan JM, Rines JEB, Osborn TR, Twardowski MS (2001) Temporal and spatial occurrence of thin phytoplankton layers in relation to physical processes. Mar Ecol Prog Ser 223:61–71CrossRefGoogle Scholar
  14. Emlet RB (1986) Larval production, dispersal, and growth in a fjord: a case study on larvae of the sand dollar Dendraster excentricus. Mar Ecol Prog Ser 31:245–254CrossRefGoogle Scholar
  15. Espinel-Velasco N, Hoffmann L, Agüera A, Byrne M, Dupont S, Uthicke S, Webster NS, Lamare M (2018) Effects of ocean acidification on the settlement and metamorphosis of marine invertebrate and fish larvae: a review. Mar Ecol Prog Ser 606:237–257CrossRefGoogle Scholar
  16. Feely RA, Sabine CL, Hernandez-Ayon JM, Ianson D, Hales B (2008) Evidence for upwelling of corrosive “acidified” water onto the continental shelf. Science 320:1490–1492PubMedCrossRefPubMedCentralGoogle Scholar
  17. Feely RA, Alin SR, Jan Newton, Sabine CL, Warner M, Devol A, Krembs C, Maloy C (2010) The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Estuar Coast Shelf Sci 88:442–449CrossRefGoogle Scholar
  18. Frieder CA, Nam SH, Martz TR, Levin LA (2012) High temporal and spatial variability of dissolved oxygen and pH in a nearshore California kelp forest. Biogeosciences 9:3917–3930CrossRefGoogle Scholar
  19. Gaitán-Espitia JD, Villanueva PA, Lopez J, Torres R, Navarro JM, Bacigalupe LD (2017) Spatio-temporal environmental variation mediates geographical differences in phenotypic responses to ocean acidification. Biol Lett 13:20160865PubMedPubMedCentralCrossRefGoogle Scholar
  20. Gallego R, Dennis TE, Basher Z, Lavery S, Sewell MA (2017) On the need to consider multiphasic sensitivity of marine organisms to climate change: a case study of the Antarctic acorn barnacle. J Biogeogr 44:2165–2175CrossRefGoogle Scholar
  21. Guadayol O, Silbiger NJ, Donahue MJ, Thomas FIM (2014) Patterns in temporal variability of temperature, oxygen and pH along an environmental gradient in a coral reef. PLoS One 9:e85213.  https://doi.org/10.1371/journal.pone.0085213 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hanson AK Jr, Donaghay PL (1998) Micro- to fine-scale chemical gradients and layers in stratified coastal waters. Oceanography 11:10–17CrossRefGoogle Scholar
  23. Hendriks IE, Olsen YS, Ramajo L, Basso L, Steckbauer A, Moore TS, Howard J, Duarte CM (2014) Photosynthetic activity buffers ocean acidification in seagrass meadows. Biogeosciences 11:333–346CrossRefGoogle Scholar
  24. Hodin J, Ferner MC, Ng G, Gaylord B (2018) Sand dollar larvae show within-population variation in their settlement induction by turbulence. Biol Bull 235:152–166PubMedCrossRefPubMedCentralGoogle Scholar
  25. Hu M, Tseng Y-C, Su Y-H, Lein E, Lee H-G, Lee J-R, Dupont S (2017) Variability in larval gut pH regulation defines sensitivity to ocean acidification in six species of the Ambulacraria superphylum. Proc R Soc B 284:20171066PubMedCrossRefPubMedCentralGoogle Scholar
  26. Hu MY, Yan J-J, Petersen I, Himmerkus N, Bleich M, Stumpp M (2018) A SLC4 family bicarbonate transporter is critical for intracellular pH regulation and biomineralization in sea urchin embryos. Elife 7:e36600PubMedPubMedCentralCrossRefGoogle Scholar
  27. Jones EM, Fenton M, Meredith MP, Clargo NM, Ossebar S, Ducklow HW, Venables HJ, de Baar HJW (2017) Ocean acidification and calcium carbonate saturation states in the coastal zone of the West Antarctic Peninsula. Deep-Sea Res Pt II 139:181–194CrossRefGoogle Scholar
  28. Katow H, Katow T, Yoshida H, Kiyomoto M, Uemura I (2016) Immunohistochemical and ultrastructural properties of the larval ciliary band-associated strand in the sea urchin Hemicentrotus pulcherrimus. Front Zool 13:27PubMedPubMedCentralCrossRefGoogle Scholar
  29. Kerrison P, Hall-Spencer JM, Suggett DJ, Hepburn LJ, Steinke M (2011) Assessment of pH variability at a coastal CO2 vent for ocean acidification studies. Estuar Coast Shelf Sci 94:129–137CrossRefGoogle Scholar
  30. Kurihara H (2008) Effects of CO2—driven ocean acidification on the early developmental stages of invertebrates. Mar Ecol Prog Ser 373:275–284CrossRefGoogle Scholar
  31. Lacalli TG, Gilmour THJ (1990) Ciliary reversal and locomotory control in the pluteus larva of Lytechinus pictus. Phil Trans R Soc Lond B 330:391–396CrossRefGoogle Scholar
  32. Lowe AT, Bos J, Ruesink J (2019) Ecosystem metabolism drives pH variability and modulates long-term ocean acidification in the Northeast Pacific coastal ocean. Sci Rep 9:963.  https://doi.org/10.1038/s41598-018-37764-4 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Macneil KEA, Scaros AT, Croll RP, Bishop CD (2017) Differences in larval arm movements correlate with the complexity of musculature in two phylogenetically distance echinoids, Eucidaristribuloides (Cidaroidea) and Lytechinus variegatus (Euechinoidea). Biol Bull 233:111–122PubMedCrossRefPubMedCentralGoogle Scholar
  34. McManus MA, Alldredge AL, Barnard AH, Boss E, Case JF, Cowles TJ, Donaghay PL, Eisner LB, Gifford DJ, Greenlaw CF, Herren CM, Holliday DV, Johnson D, MacIntyre S, McGehee DM, Osborn TR, Perry MJ, Pieper RE, Rines JEB, Smith DC, Sullivan JM, Talbot MK, Twardowski MS, Weidemann A, Zaneveld JR (2003) Characteristics, distribution and persistence of thin layers over a 48 hour period. Mar Ecol Prog Ser 261:1–19CrossRefGoogle Scholar
  35. Merrill RJ, Hobson ES (1970) Field observations of Dendraster excentricus, a sand dollar of Western North America. Am Midl Nat 83:595–624CrossRefGoogle Scholar
  36. Metaxas A, Young CM (1998) Behaviour of echinoid larvae around sharp haloclines: effects of the salinity gradient and dietary conditioning. Mar Biol 131:443–459CrossRefGoogle Scholar
  37. Murray JW, Roberts E, Howard E, O’Donnell M, Bantam C, Carrington E, Foy M, Paul B, Fay A (2015) An island sea high nitrate-low chlorophyll (HNLC) region with naturally high pCO2. Limnol Oceanogr 60:957–966CrossRefGoogle Scholar
  38. Pan T-CF, Applebaum SL, Manahan DT (2015) Experimental ocean acidification alters the allocation of metabolic energy. Proc Natl Acad Sci USA 112:4696–4701PubMedCrossRefPubMedCentralGoogle Scholar
  39. Pechenik JA (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Mar Ecol Prog Ser 177:269–297CrossRefGoogle Scholar
  40. Pennington JT, Emlet RB (1986) Ontogenetic and diel vertical migration of a planktonic echinoid larva, Dendraster excentricus (Eschsholtz): occurrence, causes and probable consequences. J Exp Mar Biol Ecol 104:69–95CrossRefGoogle Scholar
  41. Podolsky RD, Emlet RB (1993) Separating the effects of temperature and viscosity on swimming and water movement by sand dollar larvae (Dendraster excentricus). J Exp Biol 176:207–221Google Scholar
  42. Saba GK, Wright-Fairbanks E, Miles TN, Chen B, Cai W-J, Wang K, Barnard AH, Branham CW, Jones CP (2018) Developing a profiling glider pH sensor for high resolution coastal ocean acidification monitoring. OCEANS 2018 MTS/IEEE Charleston, Charleston, SC, pp. 1–8Google Scholar
  43. Sameoto JA, Metaxas A (2008a) Interactive effects of haloclines and food patches on the vertical distribution of 3 species of temperate invertebrate larvae. J Exp Mar Biol Ecol 367:131–141CrossRefGoogle Scholar
  44. Sameoto JA, Metaxas A (2008b) Can salinity-induced mortality explain larval vertical distribution with respect to a halocline? Biol Bull 214:329–338PubMedCrossRefPubMedCentralGoogle Scholar
  45. Sorte CJB, Pandori LLM, Cai S, Davis KA (2018) Predicting persistence in benthic marine species with complex life cycles: linking dispersal dynamics to redistribution potential and thermal tolerance limits. Mar Biol 165:20CrossRefGoogle Scholar
  46. Strathmann MF (1987) Reproduction and development of marine invertebrates of the northern Pacific coast: data and methods for the study of eggs, embryos, and larvae. University of Washington Press, WashingtonGoogle Scholar
  47. Stumpp M, Hu MY, Melzner F, Gutowska MA, Dorey N, Himmerkus N, Holtmann WC, Dupont ST, Thorndyke MC, Bleich M (2012) Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification. Proc Natl Acad Sci USA 109:18192–18197PubMedCrossRefPubMedCentralGoogle Scholar
  48. Timko PL (1976) Sand dollars as suspension feeders: a new description of feeding in Dendrasterexcentricus. Biol Bull 151:247–259CrossRefGoogle Scholar
  49. Wada Y, Mogami Y, Baba S (1997) Modification of ciliary beating in sea urchin larvae induced by neurotransmitters: beat-plane rotation and control of frequency fluctuation. J Exp Biol 200:9–18PubMedPubMedCentralGoogle Scholar
  50. Watson S-A, Fields JB, Munday PL (2017) Ocean acidification alters predator behaviour and reduces predation rate. Biol Lett 13:20160797PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Elizaldy A. Maboloc
    • 1
    • 2
    Email author
  • Grant Batzel
    • 2
    • 3
  • Daniel Grünbaum
    • 2
    • 4
  • Kit Yu Karen Chan
    • 1
    • 5
  1. 1.Hong Kong University of Science and TechnologyKowloonHong Kong, SAR
  2. 2.Friday Harbor LaboratoriesUniversity of WashingtonFriday HarborUSA
  3. 3.Scripps Institution of OceanographyUniversity of California San DiegoLa JollaUSA
  4. 4.School of OceanographyUniversity of WashingtonSeattleUSA
  5. 5.Department of BiologySwarthmore CollegeSwarthmoreUSA

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