Abstract
Ova of the Antarctic ascidian Cnemidocarpa verrucosa were mature at 240–245 μm. At 0 to −1.5°C, embryos hatched as swimming tadpoles at 8 days from fertilization, which is close to the ages at which some Antarctic echinoderm and nemertean embryos hatch as blastulae. Comparisons of Antarctic and temperate ascidian larvae suggest that the ascidian’s development rate is affected by low environmental temperatures to about the same extent as embryos and larvae of an echinoid, nemertean, and calanoid copepods. The ascidian’s tadpoles were bright orange and large, >2 mm in length including tunic and >1.5 mm in length without tunic. The large and brightly colored tadpoles were conspicuous when swimming, which supports the hypothesis that larvae of C. verrucosa are chemically defended against predators. Metamorphosed juveniles were found in cultures within 16 days from fertilization, when some unsettled tadpoles still moved but were less active. The potential pelagic period may therefore be 16 or more days with 8 days as an unhatched embryo and up to 8 or more days as a tadpole. The resting metabolic rate of tadpole larvae was 15 pmol O2 h−1 individual−1 which is equivalent to larval respiration rates in Antarctic echinoderms. A low resting metabolic rate suggests a potential mechanism for the extended larval lifespan in C. verrucosa.
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References
Bennett CE, Marshall DJ (2005) The relative energetic costs of the larval period, larval swimming and metamorphosis for the ascidian Diplosoma listerianum. Mar Freshw Behav Physiol 38:21–29
Berrill NJ (1935) Studies in tunicate development part III—differential retardation and acceleration. Phil Trans R Soc Lond B 225:255–326
Berrill NJ (1950) The Tunicata with an account of the British species. Bernard Quaritch, London
Bosch I (1989) Contrasting modes of reproduction in two Antarctic asteroids of the genus Porania, with a description of unusual feeding and non-feeding larval types. Biol Bull 177:77–82
Bosch I, Beauchamp KA, Steele ME, Pearse JS (1987) Development, metamorphosis, and seasonal abundance of embryos and larvae of the Antarctic sea urchin Sterechinus neumayeri. Biol Bull 173:126–135
Clarke A (1983) Life in cold water: the physiological ecology of polar marine ectotherms. Oceanogr Mar Biol Annu Rev 21:341–453
Clarke A (1992) Reproduction in the cold: Thorson revisited. Invert Reprod Dev 22:175–184
Clarke A (1998) Temperature and energetics: an introduction to cold ocean physiology. In: Portner HO, Somero GN (eds) Cold ocean physiology. Cambridge University Press, Cambridge, pp 3–32
Clarke A, Fraser KPP (2004) Why does metabolism scale with temperature? Funct Ecol 18:243–251
Emlet R, McEdward LR, Strathmann RR (1987) Echinoderm larval ecology viewed from the egg. In: Jangoux M, Lawrence JM (eds) Echinoderm studies 2. Balkema, Rotterdam, pp 145–156
Gnaiger E (1983) Calculation of energetic and biochemical equivalents of respiratory oxygen consumption. In: Gnaiger E, Forstner H (eds) Polarographic oxygen sensors. Springer, Berlin Heidelberg New York, pp 337–345
Hoegh-Guldberg O, Pearse JS (1995) Temperature, food availability, and the development of marine invertebrate larvae. Am Zool 35:415–425
Jablonski D (1986) Larval ecology and macroevolution in marine invertebrates. Bull Mar Sci 39:565–587
Knox GA, Waghorn EJ, Ensor PH (1996) Summer plankton beneath the McMurdo Ice Shelf at White Island, McMurdo Sound, Antarctica. Polar Biol 16:87–94
Kume M, Dan K (1966) Invertebrate embryology. NOLIT, Belgrade
Lindquist N, Hay ME, Fenical W (1992) Defense of ascidians and their conspicuous larvae: adult vs. larval chemical defenses. Ecol Monogr 62:547–568
Marsh AG, Cohen S, Epifanio CE (2001) Larval energy metabolism and physiological variability in the Asian shore crab, Hemigrapsus sanguineus. Mar Ecol Prog Ser 218:303–309
Marsh AG, Leong P, Manahan DT (1999) Energy metabolism during embryonic development and larval growth of an Antarctic sea urchin. J Exp Biol 202:2041–2050
Marsh AG, Maxson RE, Manahan DT (2001) High macromolecular synthesis with low metabolic cost in Antarctic sea urchin embryos. Science 291:1950–1952
Marshall DJ, Styan CA, Keough MJ (2000) Intraspecfic co-variation between egg and body size affects fertilization kinetics of free-spawning marine invertebrates. Mar Ecol Prog Ser 195:305–309
McClintock JB, Baker BJ (1997) Palatability and chemical defense of eggs, embryos and larvae of shallow-water antarctic marine invertebrates. Mar Ecol Prog Ser 154:121–131
McClintock JB, Heine J, Slattery M, Weston J (1991) Biochemical and energetic composition, population biology, and chemical defense of the antarctic ascidian Cnemidocarpa verrucosa Lesson. J Exp Mar Biol Ecol 147:163–175
McLaren IA, Corkett CJ, Zillioux EJ (1969) Temperature adaptations of copepod eggs from the Arctic to the Tropics. Biol Bull 137:486–493
McLaren IA, Sévigny J-M, Corkett CJ (1989) Temperature-dependent development in Pseudocalanus species. Can J Zool 67:559–564
Mileikovsky SA (1971) Types of larval development in marine bottom invertebrates, their distribution and ecological significance: a reevaluation. Mar Biol 10:193–213
Park YJ, Rho YG, Lee JH, Lee JM (1991) Studies on spawning and seed collection of sea squirt, Halocynthia roretzi (Drasche). Bull Natl Fish Res Dev Agency (Korea) 45:165–173
Pearse JS (1994) Cold-water echinoderms break “Thorson’s Rule”. In: Eckelbarger KJ, Young CM (eds) Reproduction, larval biology and recruitment in deep-sea benthos. Columbia University Press, New York, pp 26–43
Pearse JS, Lockhart SJ (2004) Reproduction in cold water: paradigm changes in the 20th century and a role for cidaroid sea urchins. Deep-Sea Res II 51:1533–1549
Pearse JS, McClintock JB, Bosch I (1991) Reproduction of Antarctic benthic marine-invertebrates - tempos, modes, and timing. Am Zool 31:65–80
Peck LS (1993) Larval development in the Antarctic nemertean Parborlasia corrugatus (Heteronemertea: Lineidae). Mar Biol 116:301–310
Peck LS (2002) Ecophysiology of Antarctic marine ectotherms: limits to life. Polar Biol 25:31–40
Peck LS, Prothero-Thomas E (2002) Temperature effects on the metabolism of larvae of the Antarctic starfish Odontaster validus, using a novel microrespirometry method. Mar Biol 141:271–276
Sahade R, Tatián M, Esnal GB (2004) Reproductive ecology of the ascidian Cnemidocarpa verrucosa at Potter Cove, South Shetland Islands, Antarctica. Mar Ecol Prog Ser 272:131–140
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
Staver JM, Strathmann RR (2002) Evolution of fast development of embryos to early swimming. Biol Bull 203:58–69
Strathmann RR, Staver JM, Hoffman JR (2002) Risk and the evolution of cell cycle durations of embryos. Evolution 56:708–720
Szela TL, Marsh AG (2005) Microtiter plate, optrode respirometry reveals large interindividual variance in metabolic rates among individual nauplii of Artemia sp. Mar Ecol Prog Ser 296:281–289
Tatián M, Sahade R, Kowalke J, Kivatinitz SC, Esnal GB (2002) Food availability and gut contents in the ascidian Cnemidocarpa verrucosa at Potter Cove, Antactica. Polar Biol 25:58–64
Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45
Vorontsova MN, Malakhov VV (1984) Anatomy and fine structure of larvae in the ascidan Cnemidocarpa finmarkiensis (Stolidobranchia, Styelidae). 2. Sense organs. Zoologischeskii Zhurnal 63:1036–1045
Ward P, Shreeve R (1998) Egg hatching times of Antarctic copepods. Polar Biol 19:142–144
Young CM, Bingham BL (1987) Chemical defense and aposematic coloration in larvae of the ascidian Ecteinascidia turbinata. Mar Biol 96:539–544
Acknowledgements
The research was supported by NSF grants OPP 0238281 to A. G. Marsh and OCE 0217304 to R. R. Strathmann. We are grateful to C. Lambert, J. B. McClintock, F. Monniot, J. S. Pearse, and R. Sahade for advice and information and to P. Ulrich, R. Robbins, and other scientists and staff at McMurdo Station for help with the research.
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Strathmann, R.R., Kendall, L.R. & Marsh, A.G. Embryonic and larval development of a cold adapted Antarctic ascidian. Polar Biol 29, 495–501 (2006). https://doi.org/10.1007/s00300-005-0080-7
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DOI: https://doi.org/10.1007/s00300-005-0080-7