Effect of near-future seawater temperature rises on sea urchin sperm longevity
M. T. Binet A C and C. J. Doyle B
+ Author Affiliations
- Author Affiliations
A Centre for Environmental Contaminants Research, CSIRO Land and Water, Locked Bag 2007, Kirrawee, Sydney, NSW 2232, Australia.
B Ecotox Services Australasia, 27/2 Chaplin Drive, Lane Cove, NSW 2066, Australia.
C Corresponding author. Email: monique.binet@csiro.au
Marine and Freshwater Research 64(1) 1-9 https://doi.org/10.1071/MF12121
Submitted: 1 May 2012 Accepted: 19 October 2012 Published: 6 February 2013
Abstract
Global warming has and will continue to warm the world’s oceans, which may have detrimental consequences for marine life. Studies assessing the impact of climate-change stressors on early life-stages of marine invertebrates have focussed on immediate fertilisation success or larval development, but have so far not considered gamete longevity. Recent studies have suggested that sea urchin fertilisation can take place for several hours, as dilute spermatozoa can travel to fertilise distant eggs, making gamete longevity an important factor in fertilisation success for some species. The longevity of spermatozoa from Heliocidaris tuberculata was assessed over a 3-h exposure to current ambient (20°C), near-future (24°C) and future (26°C) ocean-temperature scenarios. Sperm mitochondrial activity was also measured throughout the 3-h exposure using the stain Rhodamine 123 (Rh123) and flow cytometry. Sperm longevity, based on fertilisation success, significantly decreased following a 1-h exposure at 26°C, or a 3-h exposure at 24°C, relative to the 20°C treatment. However, sperm mitochondrial activity did not correlate with fertilisation success. Even when fertilisation success was below 20%, Rh123 uptake remained above 80%, indicating the presence of active mitochondria in non-viable spermatozoa. Our results suggested that at projected sea-surface temperatures, the longevity of sea urchin spermatozoa is reduced, which may have consequences for sea urchin population dynamics.
Additional keywords: climate change, fertilisation, flow cytometry, marine invertebrate, Rhodamine 123.
References
Adams, S. L., Hessian, P. A., and Mladenov, P. V. (2003). Flow cytometric evaluation of mitochondrial function and membrane integrity of marine invertebrate sperm. Invertebrate Reproduction & Development 44, 45–51.| Flow cytometric evaluation of mitochondrial function and membrane integrity of marine invertebrate sperm.Crossref | GoogleScholarGoogle Scholar |
Byrne, M. (2010). Impact of climate change stressors on marine invertebrate life histories with a focus on the Mollusca and Echinodermata. In ‘Climate Alert: Climate Change Monitoring and Strategy’ (Ed. Y. Yuzhu.) pp. 142–185. (University of Sydney Press: Sydney.)
Byrne, M. (2012). Global change ecotoxicology: identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Marine Environmental Research 76, 3–15.
| Global change ecotoxicology: identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvV2iurk%3D&md5=c0832b107c0518022ffd03e8071c2830CAS |
Byrne, M., Soars, N. A., Ho, M. A., Wong, E., McElroy, D., Selvakumaraswamy, P., Dworjanyn, S. A., and Davis, A. R. (2010). Fertilization in a suite of coastal marine invertebrates from SE Australia is robust to near-future ocean warming and acidification. Marine Biology 157, 2061–2069.
| Fertilization in a suite of coastal marine invertebrates from SE Australia is robust to near-future ocean warming and acidification.Crossref | GoogleScholarGoogle Scholar |
Byrne, M., Selvakumaraswamy, P., Ho, M. A., Woolsey, E., and Nguyen, H. D. (2011). Sea urchin development in a global change hotspot, potential for southerly migration of thermotolerant propagules. Deep-sea Research. Part II, Topical Studies in Oceanography 58, 712–719.
| Sea urchin development in a global change hotspot, potential for southerly migration of thermotolerant propagules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXit1aqsbk%3D&md5=a0abdab889055fa04fb7b529077efe26CAS |
Chia, F.-S., and Bickell, L. R. (1983). Echinodermata. In ‘Reproductive Biology of Invertebrates. V.2. Spermatogenesis and Sperm Function’. (Eds K. G. Adiyodi and R. G. Adiyodi.) pp. 545–620. (John Wiley and Sons: Chichester, UK.)
Christen, R., Schackmann, R. W., and Shapiro, B. M. (1983). Metabolism of sea urchin sperm: interrelationships between intracellular pH, ATPase activity and mitochondrial respiration. The Journal of Biological Chemistry 258, 5392–5399.
| 1:CAS:528:DyaL3sXitFegt7w%3D&md5=83abe6d2c50ab10b8f41355803ab3aaaCAS |
Christen, R., Schackmann, R. W., and Shapiro, B. M. (1986). Ionic regulation of sea urchin sperm motility, metabolism and fertilizing capacity. The Journal of Physiology 379, 347–365.
| 1:CAS:528:DyaL28Xls12gsbo%3D&md5=b41b9c586d7ed023ee9ef10278707ae2CAS |
Cosson, J., Groison, A.-L., Suquet, M., Fauvel, C., and Billard, R. (2008). Studying sperm motility in marine fish: an overview on the state of the art. Journal of Applied Ichthyology 24, 460–486.
| Studying sperm motility in marine fish: an overview on the state of the art.Crossref | GoogleScholarGoogle Scholar |
De Baulny, B. O., Le Vern, Y., Kerboeuf, D., and Maisse, G. (1997). Flow cytometric evaluation of mitochondrial activity and membrane integrity in fresh and cryopreserved rainbow trout (Ochorhynchus mykiss) spermatozoa. Cryobiology 34, 141–149.
| Flow cytometric evaluation of mitochondrial activity and membrane integrity in fresh and cryopreserved rainbow trout (Ochorhynchus mykiss) spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Denny, M. W., and Shibata, M. F. (1989). Consequences of surf-zone turbulence for settlement and external fertilization. American Naturalist 134, 859–889.
| Consequences of surf-zone turbulence for settlement and external fertilization.Crossref | GoogleScholarGoogle Scholar |
Dinnel, P. A., Link, J. M., Stober, Q. J., Letourneau, M. W., and Roberts, W. E. (1989). Comparative sensitivity of sea urchin sperm bioassays to metals and pesticides. Archives of Environmental Contamination and Toxicology 18, 748–755.
| Comparative sensitivity of sea urchin sperm bioassays to metals and pesticides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlsVygtLo%3D&md5=e0b0f6bcb962bd85f3406f55e7cdbf27CAS |
Edgar, G. J. (1997). ‘Australian Marine Life. The Plants and Animals of Temperate Waters.’ (Reed Books: Melbourne.)
Figueira, W. F., and Booth, D. J. (2010). Increasing ocean temperatures allow tropical fishes to survive overwinter in temperate waters. Global Change Biology 16, 506–516.
| Increasing ocean temperatures allow tropical fishes to survive overwinter in temperate waters.Crossref | GoogleScholarGoogle Scholar |
Fujisawa, H., and Shigei, M. (1990). Correlation of embryonic temperature sensitivity of sea urchins with spawning season. Journal of Experimental Marine Biology and Ecology 136, 123–139.
| Correlation of embryonic temperature sensitivity of sea urchins with spawning season.Crossref | GoogleScholarGoogle Scholar |
Gambaiani, D. D., Mayol, P., Isaac, S. J., and Simmonds, M. P. (2009). Potential impacts of climate change and greenhouse gas emissions on Mediterranean marine ecosystems and cetaceans. Journal of the Marine Biological Association of the United Kingdom 89, 179–201.
| Potential impacts of climate change and greenhouse gas emissions on Mediterranean marine ecosystems and cetaceans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1ahs7c%3D&md5=aedd1ddad60454d2d8de9ac3aebc2235CAS |
Gillan, L., Evans, G., and Maxwell, W. M. C. (2005). Flow cytometric evaluation of sperm parameters in relation to fertility potential. Theriogenology 63, 445–457.
| Flow cytometric evaluation of sperm parameters in relation to fertility potential.Crossref | GoogleScholarGoogle Scholar |
Graham, J. K. (2001). Assessment of sperm quality: a flow cytometric approach. Animal Reproduction Science 68, 239–247.
| Assessment of sperm quality: a flow cytometric approach.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MnpslKntw%3D%3D&md5=0af6a0ffc5118d468757c00af6481a7aCAS |
Graham, C. T., and Harrod, C. (2009). Implications of climate change for the fishes of the British Isles. Journal of Fish Biology 74, 1143–1205.
| Implications of climate change for the fishes of the British Isles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cjnt1ygug%3D%3D&md5=052496d75899d8085557431b64314099CAS |
Hart, M. W. (2002). Life history evolution and comparative developmental biology of echinoderms. Evolution and Development 4, 62–71.
| Life history evolution and comparative developmental biology of echinoderms.Crossref | GoogleScholarGoogle Scholar |
IPCC (International Panel on Climate Change) (2007). ‘The Fourth Assessment Report of the IPCC.’ (Cambridge University Press: Cambridge, UK.)
Johnson, S. L., and Yund, P. O. (2004). Remarkable longevity of dilute sperm in a free-spawning colonial ascidian. The Biological Bulletin 206, 144–151.
| Remarkable longevity of dilute sperm in a free-spawning colonial ascidian.Crossref | GoogleScholarGoogle Scholar |
Johnson, C. R., Banks, S. C., Barrett, N. S., Cazassus, F., Dunstan, P. K., Edgar, G. J., Frusher, S. D., Gardner, C., Haddon, M., Helidoniotis, F., Hill, K. L., Holbrook, N. J., Hosie, G. W., Last, P. R., Ling, S. D., Melbourne-Thomas, J., Miller, K., Pecl, G. T., Richardson, A. J., Ridgway, K. R., Rintoul, S. R., Ritz, D. A., Ross, D. J., Sanderson, J. C., Shepherd, S. A., Slotwinski, A., Swadling, K. M., and Taw, N. (2011). Climate change cascades: Shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania. Journal of Experimental Marine Biology and Ecology 400, 17–32.
| Climate change cascades: Shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania.Crossref | GoogleScholarGoogle Scholar |
Laegdsgaard, P., Byrne, M., and Anderson, D. T. (1991). Reproduction of sympatric populations of Heliocidaris erythrogramma and H. tuberculata (Echinoidea) in New South Wales. Marine Biology 110, 359–374.
| Reproduction of sympatric populations of Heliocidaris erythrogramma and H. tuberculata (Echinoidea) in New South Wales.Crossref | GoogleScholarGoogle Scholar |
Lauzon-Guay, J., and Scheibling, R. E. (2007). Importance of spatial population characteristics on the fertilization rates of sea urchins. The Biological Bulletin 212, 195–205.
| Importance of spatial population characteristics on the fertilization rates of sea urchins.Crossref | GoogleScholarGoogle Scholar |
Levitan, D. R. (2000). Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegates. Proceedings of the Royal Society of London. Series B. Biological Sciences 267, 531–534.
| Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegates.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3ks1ygtg%3D%3D&md5=97a7b7e51067768e993943b7e644cc9fCAS |
Levitan, D. R., and Petersen, C. (1995). Sperm limitation in the sea. Trends in Ecology & Evolution 10, 228–231.
| Sperm limitation in the sea.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFansQ%3D%3D&md5=8304b0ef6b2acaec4264e67979ac64a7CAS |
Levitan, D. R., Sewell, M. A., and Chia, F. (1991). Kinetics of fertilization in the sea urchin Strongylocentrotus franciscannus: interaction of gamete dilution, age, and contact time. The Biological Bulletin 181, 371–378.
| Kinetics of fertilization in the sea urchin Strongylocentrotus franciscannus: interaction of gamete dilution, age, and contact time.Crossref | GoogleScholarGoogle Scholar |
Levitan, D. R., Sewell, M. A., and Chia, F. S. (1992). How distribution and abundance influence fertilization success in the sea-urchin Strongylocentrotus franciscanus. Ecology 73, 248–254.
| How distribution and abundance influence fertilization success in the sea-urchin Strongylocentrotus franciscanus.Crossref | GoogleScholarGoogle Scholar |
Lu, X. Y., and Wu, R. S. S. (2005). Ultraviolet damages sperm mitochondrial function and membrane integrity in the sea urchin Anthocidaris crassispina. Ecotoxicology and Environmental Safety 61, 53–59.
| Ultraviolet damages sperm mitochondrial function and membrane integrity in the sea urchin Anthocidaris crassispina.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtVyktrk%3D&md5=d86b5038fa90bb02c2fc6f0cb5843f62CAS |
Manríquez, P. H., Hughes, R. N., and Bishop, J. D. D. (2001). Age-dependant loss of fertility in water-borne sperm of the bryozan Celleporella hyaline. Marine Ecology Progress Series 224, 87–92.
| Age-dependant loss of fertility in water-borne sperm of the bryozan Celleporella hyaline.Crossref | GoogleScholarGoogle Scholar |
Martínez-Pastor, F., Mata-Campuzano, M., Alvarez-Rodriguez, M., Alvarez, M., Anel, L., and de Paz, P. (2010). Probes and techniques for sperm evaluation by flow cytometry. Reproduction in Domestic Animals 45, 67–78.
| Probes and techniques for sperm evaluation by flow cytometry.Crossref | GoogleScholarGoogle Scholar |
Meidel, S. K., and Yund, P. O. (2001). Egg longevity and time-integrated fertilization in a temperate sea urchin (Strongylocentrotus droebachiensis). The Biological Bulletin 201, 84–94.
| Egg longevity and time-integrated fertilization in a temperate sea urchin (Strongylocentrotus droebachiensis).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mvot1OnsA%3D%3D&md5=456bf570e2cd19803de45bd25d61f63dCAS |
Mita, M., and Nakamura, M. (1998). Energy metabolism of sea urchin spermatozoa: an approach based on echinoid phylogeny. Zoological Science 15, 1–10.
| Energy metabolism of sea urchin spermatozoa: an approach based on echinoid phylogeny.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjvVensr0%3D&md5=61b0e8f4c25afeff9727490c8a129095CAS |
Mita, M., Hino, A., and Yasumasu, I. (1984). Effect of temperature on interaction between eggs and spermatozoa of sea urchin. The Biological Bulletin 166, 68–77.
| Effect of temperature on interaction between eggs and spermatozoa of sea urchin.Crossref | GoogleScholarGoogle Scholar |
O’Connor, C., and Mulley, J. C. (1977). Temperature effects on periodicity and embryology, with observations on the population genetics of the aquacultural echinoid Heliocidaris tuberculata. Aquaculture 12, 99–114.
| Temperature effects on periodicity and embryology, with observations on the population genetics of the aquacultural echinoid Heliocidaris tuberculata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXkslOktw%3D%3D&md5=4b02d410f74c3756742d93768816bcf7CAS |
O’Connor, C. O., Riley, G., and Bloom, D. (1976). Reproductive periodicities of the echinoids of the Solitary Islands in the light of some ecological variables II. Superficial and histological changes in the gonads of Centrostephanus rodgersii (Clark), Phyllacanthus parvispinus (Tenison-Woods), Heliocidaris tuberculata (Clark), and Tripneustes gratilla (Linneus), and their relevance to aquaculture. Thalassia Jugoslavika 12, 245–267.
Paniagua-Chávez, C. G., Jenkins, J., Segovia, M., and Tiersch, T. R. (2006). Assessment of gamete quality for the eastern oyster (Crassostrea virginica) by use of fluorescent dyes. Cryobiology 53, 128–138.
| Assessment of gamete quality for the eastern oyster (Crassostrea virginica) by use of fluorescent dyes.Crossref | GoogleScholarGoogle Scholar |
Pennington, J. T. (1985). The ecology of echinoid eggs: the consequences of sperm dilution, adult aggregation and synchronous spawning. The Biological Bulletin 169, 417–430.
| The ecology of echinoid eggs: the consequences of sperm dilution, adult aggregation and synchronous spawning.Crossref | GoogleScholarGoogle Scholar |
Pierrat, B., Saucede, T., Festau, A., and David, B. (2012). Antarctic, sub-antarctic and cold temperate echinoid database. ZooKeys 204, 47–52.
| Antarctic, sub-antarctic and cold temperate echinoid database.Crossref | GoogleScholarGoogle Scholar |
Poloczanska, E. S., Babcock, R. C., Butler, A., Hobday, A. J., Hoegh-Guldberg, O., Kunz, T. J., Matear, R., Milton, D. A., Okey, T. A., and Richardson, A. J. (2007). Climate change and Australian marine life. Oceanography and Marine Biology 45, 407–478.
Przeslawski, R., Ahyong, S., Byrne, M., Woerheide, G., and Hutchings, P. (2008). Beyond corals and fish: the effects of climate change on non-coral benthic invertebrates of tropical reefs. Global Change Biology 14, 2773–2795.
| Beyond corals and fish: the effects of climate change on non-coral benthic invertebrates of tropical reefs.Crossref | GoogleScholarGoogle Scholar |
Rahman, S., Tsuchiya, M., and Uehara, T. (2009a). Effects of temperature on gamete longevity and fertilization success in two sea urchin species, Echinometra mathaei and Tripneustes gratilla. Zoological Science 26, 1–8.
| Effects of temperature on gamete longevity and fertilization success in two sea urchin species, Echinometra mathaei and Tripneustes gratilla.Crossref | GoogleScholarGoogle Scholar |
Rahman, S., Tsuchiya, M., and Uehara, T. (2009b). Effects of temperature on hatching rate, embryonic development and early larval survival of the edible sea urchin Tripneustes gratilla. Biologia 64, 768–775.
| Effects of temperature on hatching rate, embryonic development and early larval survival of the edible sea urchin Tripneustes gratilla.Crossref | GoogleScholarGoogle Scholar |
Ridgeway, K. R. (2007). Long-term trend and decadal variability of the southward penetration of the East Australian Current. Geophysical Research Letters 34, .
| Long-term trend and decadal variability of the southward penetration of the East Australian Current.Crossref | GoogleScholarGoogle Scholar |
Ruiz-Pesini, E., Diez-Sanchez, C., Lopez-Perez, M. J., and Enriquez, J. A. (2007). The role of the mitochondrion in sperm function: is there a place for oxidative phosphorylation or is this a purely glycolytic process? Current Topics in Developmental Biology 77, 3–19.
| The role of the mitochondrion in sperm function: is there a place for oxidative phosphorylation or is this a purely glycolytic process?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1GltLY%3D&md5=583656a69a94648b2754d948e7a7835eCAS |
Sewell, M. A., and Young, C. G. (1999). Temperature limits to fertilization and early development in the tropical sea urchin Echinometra lucunter. Journal of Experimental Marine Biology and Ecology 236, 291–305.
| Temperature limits to fertilization and early development in the tropical sea urchin Echinometra lucunter.Crossref | GoogleScholarGoogle Scholar |
Southward, A. J., Hawkins, S. J., and Burrows, M. T. (1995). Seventy years’ observations of changes in distribution and abundance of zooplankton and intertidal organisms in the Western English Channel in relation to rising sea temperature. Journal of Thermal Biology 20, 127–155.
| Seventy years’ observations of changes in distribution and abundance of zooplankton and intertidal organisms in the Western English Channel in relation to rising sea temperature.Crossref | GoogleScholarGoogle Scholar |
Spiegler, M. A., and Oppenheimer, S. B. (1995). Extending the viability of sea urchin gametes. Cryobiology 32, 168–174.
| Extending the viability of sea urchin gametes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M3mt1CnsA%3D%3D&md5=1c78972cb260cd9e4cf3a932d617d7d4CAS |
Suquet, M., Billard, R., Cosson, J., Normant, Y., and Fauvel, C. (1995). Artificial insemination in turbot (Scophthalmus maximus): determination of the optimal sperm to egg ratio and time of gamete contact. Aquaculture 133, 83–90.
| Artificial insemination in turbot (Scophthalmus maximus): determination of the optimal sperm to egg ratio and time of gamete contact.Crossref | GoogleScholarGoogle Scholar |
Thomas, F. (1994). Physical-properties of gametes in 3 sea-urchin species. The Journal of Experimental Biology 194, 263–284.
Wahle, R. A., and Gilbert, A. E. (2002). Detecting and quantifying male sea urchin spawning with time-integrated fertilization assays. Marine Biology 140, 375–382.
| Detecting and quantifying male sea urchin spawning with time-integrated fertilization assays.Crossref | GoogleScholarGoogle Scholar |
Wahle, R. A., and Peckham, S. H. (1999). Density-related reproductive trade-offs in the green sea urchin, Strongylocentrotus droebachiensis. Marine Biology 134, 127–137.
| Density-related reproductive trade-offs in the green sea urchin, Strongylocentrotus droebachiensis.Crossref | GoogleScholarGoogle Scholar |
Walther, G.-R., Post, E., Convey, P., Menzel, A., Parmesani, C., Beebee, T. J. C., Fromentin, J.-M., Hoegh-Guldberg, O., and Bairlein, F. (2002). Ecological responses to recent climate change. Nature 416, 389–395.
| Ecological responses to recent climate change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XislantL8%3D&md5=adc1292a2bf437e0e8b30d718110cfdfCAS |
Wernberg, T., Russel, B. D., Moore, P. J., Ling, S. D., Smale, D. A., Campbell, A., Coleman, M. A., Steinberg, P. D., Kendrick, G. A., and Connel, S. D. (2011). Impacts of climate change in a global hotspot for temperate marine biodiversity and ocean warming. Journal of Experimental Marine Biology and Ecology 400, 7–16.
| Impacts of climate change in a global hotspot for temperate marine biodiversity and ocean warming.Crossref | GoogleScholarGoogle Scholar |
Williams, M. E., and Bentley, M. G. (2002). Fertilization success in marine invertebrates: the influence of gamete age. The Biological Bulletin 202, 34–42.
| Fertilization success in marine invertebrates: the influence of gamete age.Crossref | GoogleScholarGoogle Scholar |
Yund, P. O., and Meidel, S. K. (2003). Sea urchin spawning in benthic boundary layers: are eggs fertilized before advecting away from females? Limnology and Oceanography 48, 795–801.
| Sea urchin spawning in benthic boundary layers: are eggs fertilized before advecting away from females?Crossref | GoogleScholarGoogle Scholar |
