Temperature and the larval ecology of the crown-of-thorns starfish, Acanthaster planci.
Population outbreaks of Acanthaster on the GBR have occurred over some 1000 km of reef (6 degrees of latitude). The main wave of outbreaks declined at around 20 [degrees] S (18), which lies to the south of Davies Reef; only a few smaller outbreaks are now being recorded at the far southern end of the system in the Swain complex (1). Lucas (2) has hypothesized that southern limits of Acanthaster's distribution may be dictated by larval temperature requirements. However, Acanthaster occurs in cooler waters near the limits of hard coral distribution (3, 4, 7). Temporally variable aggregations of Acanthaster at some Japanese sites appear to be derived entirely from settlement of larvae carried by currents from warmer water areas (19), but at other cooler water sites there are relatively stable Acanthaster populations. For example, there is evidence of increasing Acanthaster numbers at Lord Howe Island (20), although the mean surface water temperature there during January, the warmest month of the year, is about 24 [degrees] C, which is below the reported range of developmental temperature tolerance. Population maintenance there conceivably could depend solely upon recruitment of larvae carried by currents from the GBR, but the Lord Howe Island population is genetically divergent from GBR populations (21), and gene flow into it from the GBR appears to be very limited, indicating a relatively isolated, locally reproducing population. Such evidence of successful reproduction under diverse environmental temperature regimes and genetic evidence for long-distance larval transport (14) suggest complexity in Acanthaster's developmental temperature relationships. We have investigated both the developmental temperature tolerances of offspring of geographically widely separated groups of Acanthaster and the effects of experimentally altering temperature exposures of adult, embryonic, and larval starfish.
Offspring of animals collected off the Gove Peninsula near Nhulunbuy and at Davies Reef in the GBR completed development to bipinnaria larvae equally well at 31 [degrees], 27 [degrees], and 24 [degrees] C. At 22.3 [degrees] and 21 [degrees] C, Davies Reef embryos produced normal bipinnariae. At the same temperatures, some Gove embryos hatched, but they ceased development as abnormal early gastrulae.
Such geographic differences in developmental temperature tolerance may be due to genetic differentiation of separated populations, physiological acclimatization effects reflecting recent parental temperature exposure, or a combination of the two (22-24). We conducted a laboratory acclimation experiment to investigate a possible parental acclimatization effect in Acanthaster. A group of adults from Davies Reef was separated into two samples. One sample was held for 18 days at 31 [degrees] C and the other at 25 [degrees] C for 21 days. We observed differences between the offspring of 25 [degrees]-acclimated animals and 31 [degrees]-acclimated animals in tolerance to lower temperatures and in early cleavage rates, which in other echinoderms are proportional to overall developmental rates at least to the gastrula stage (25). The tolerance difference indicates an acclimatory translation of tolerance range, but more data at several temperatures would be needed to determine if the observed rate difference resulted from rotation of the rate: temperature curve.
We also examined possible parental effects due to seasonal change in water temperature in animals studied immediately after collection at Davies Reef in October (temperature at collection site: 25.5 [degrees] C) and in November (temperature: 27 [degrees] C). Offspring of the two groups differed in their tolerance to high temperature. In October-collected animals, development to early bipinnaria larvae proceeded normally between 21 [degrees] and 27 [degrees] C, but not at 32 [degrees] C. However, offspring of November-collected animals developed into normal bipinnaria at 32 [degrees]. This seasonal change resembles those reported for other echinoderms (26, 27).
Thus early developmental temperature tolerances in Acanthaster vary with recent parental temperature exposure as well as geographic source. However, our results do not distinguish the relative contributions made by population genetic differentiation and physiological acclimatization to the observed geographic variations.
Table I Development of embryos from each of four groups at low experimental temperatures Zygote to Bipinn. Zygote to Bipinn. Cleavage Group DAVIES + + none GOVE -- -- none 31 [degrees]-ACCL -- -- none 25 [degrees]-ACCL + * abnormal Bipinn. = bipinnaria larva; + indicates normal development to bipinnaria larvae; - indicates failure to develop to bipinnariae; * indicates development of larvae with clumps of extra mesenchyme-like cells rarely observed in embryos developing at 31 [degrees], 27 [degrees], or 24 [degrees] C. Gamete shedding was induced by 1-methyl adenine injection. Zygotes were transferred to rearing dishes at experimental temperatures within 5 min after fertilization at room temperature (24 [degrees] C). Animals were collected off Nhulunbuy on the Gove Peninsula and at Davies Reef on 18 and 19 December 1991, and maintained in running seawater at approximately 27 [degrees] until experiments began early in January 1992. Acclimation of samples of Davies Reef animals began on 3 January 1992, and continued at 31 [degrees] C for 18 days and at 25 [degrees] C for 21 days.
Because of its importance for dispersal, the temperature tolerance of newly hatched swimming embryos was examined. Early gastrulae from cultures of Gove embryos were transferred to 21 [degrees] and 18 [degrees] C (temperatures at which Gove embryos cannot cleave normally). Transferred embryos continued to swim, completed gastrulation, and produced bipinnariae at both temperatures. This unexpectedly broad temperature tolerance in gastrula-stage embryos prompted additional transfer experiments. Newly hatched Davies Reef gastrulae transferred from 27 [degrees] to 18.5 [degrees] C developed into bipinnariae that appeared normal. Even gastrulae transferred from 27 [degrees] to 15 [degrees] C and held there for 6 days continued to swim actively, slowly continued archenteron extension, and then quickly completed bipinnaria morphogenesis after transfer back to 27 [degrees] C. However, these larvae contained clumps of extra mesenchyme-like cells.
In summary, data presented here support a modified concept of temperature tolerance during early Acanthaster development, indicating that Acanthaster's distribution and abundance need not be as limited by developmental temperature as previously thought. Clearly, temperature relationships in later larval stages should be reexamined, especially for populations at the extremes of Acanthaster's distribution. Further, the temperature tolerance of Acanthaster gastrulae adds to a list of traits that make Acanthaster larvae particularly well adapted for long-distance dispersal. Even larvae swept into cooler water could very slowly continue normal development during transport. This, along with the ability to develop at the low phytoplankton concentrations common in tropical waters (28, 29) and the negatively geotropic swimming behavior characteristic of Acanthaster gastrula (3), would allow transport to distant reef sites with conditions appropriate for later larval development and settling--processes that may be less resistant to environmental variation (2). Early larval hardiness may facilitate both the routine dispersal of larvae and the propagation of Acanthaster outbreaks.
Table II Results of gastrula transfer experiments with Gove embryos Percent Bipinn. Transfer group Days development 31 [degrees] to 31 [degrees] (Control) 2 93 31 [degrees] to 21 [degrees] 5 88 31 [degrees] to 18 [degrees] 17 81 Only swimming, newly hatched, early gastrulae were transferred. The numbers of days from transfer to final observation are given. Comparable results were obtained following transfers of embryos that developed from fertilization to hatching at 27 [degrees] C.
This work was funded by the Great Barrier Reef Marine Park Authority through the Crown-of-Thorns Starfish Research Committee. We thank C. Cartwright, K. Hall, and D. Whitehead for technical assistance, P. Moran and C. Mundy for discussion and advice, J. Quam for map preparation, and C. Christie for collecting Acanthaster at Nhulunbuy.
1. Moran, P. J., G. De'ath, V. J. Baker, D. K. Bass, C. A. Christie, I. R. Miller, B. A. Miller-Smith, and A. A. Thompson. 1992. Pattern of outbreaks of crown-of-thorns starfish (Acanthaster planci L.) along the Great Barrier reef. Pp. 555-568 in Crown-of-Thorns Starfish on the Great Barrier Reef: Reproduction, Recruitment and Hydrodynamics, C. Johnson, ed. Aust. J. Mar. Freshwater Res. 43(3).
2. Lucas, J. S. 1973. Reproductive and larval biology of Acanthaster planci in great Barrier Reef waters. Micronesica 9: 197-203.
3. Yamaguchi, M. 1973. Early life histories of coral reef asteroids, with special reference to Acanthaster planci (L.). Pp. 369-387 in Biology and Geology of Coral Reefs. Vol. 2, O. A. Jones and R. Endean, eds. Academic Press, New York.
4. McKnight, D. G. 1978. Acanthaster planci (Linnaeus) (Asteroidea: Echinodermata) at the Kermedec Islands. N. Z. Oceanogr. Inst. Rec. 4: 17-19.
5. Birkeland, C. 1989. The influence of echinoderms on coral-reef communities. Pp. 1-79 in Echinoderm Studies, Vol. 3, M. Jangoux and J. M. Lawrence, eds. A. A. Balkema, Rotterdam.
6. Zann, L. P., and P. J. Moran. 1988. A coordinated research program on the Acanthaster phenomenon. Pp. 177-182 in Proc. Sixth Int. Coral Reef Symp. Vol. 2.
7. Birkeland, C. and J. S. Lucas. 1990. Acanthaster planci: Major Management Problem of Coral Reefs. CRC Press, Boca Raton, FL.
8. Johnson, C., ed. 1992. Crown-of-Thorns Starfish on the Great Barrier Reef: Reproduction, Recruitment and Hydrodynamics. Aust. J. Mar. Freshwater Res. 43(3).
9. Walbran, P. D., R. A. Henderson, A. J. T. Jull, and M. J. Head. 1989. Evidence from sediments of long-term Acanthaster planci predation on corals of the Great Barrier reef. Science 245: 847-850.
10. Cameron, A. M., R. Endean, and L. M. DeVantier. 1991. Predation on massive corals: Are devastating population outbreaks of Acanthaster planci novel events? Mar. Ecol. Prog. Ser. 75: 251-258.
11. Moran, P. J., and R. H. Bradbury. 1989. The crown-of-thorns starfish controversy. Search 20: 3-6.
12. Reichelt, R. E., R. H. Bradbury, and P. J. Moran. 1990. Distribution of Acanthaster planci outbreaks on the Great Barrier Reef between 1966 and 1989. Coral Reefs 9: 97-103.
13. Kenchington, R. A. 1977. Growth and recruitment of Acanthaster planci (L.) on the Great Barrier Reef. Biol. Conservation 11: 103-118.
14. Benzie, J. A. H., and J. A. Stoddart. 1992. Genetic structure of outbreaking and non-outbreaking crown-of-thorns starfish (Acanthaster planci) populations on the Great Barrier Reef. Mar. Biol. 112: 119-130.
15. James, M. K., and J. P. Scandol. 1992. Larval dispersal simulations: correlation with the crown-of-thorns starfish outbreaks database. Pp. 569-582 in Crown-of-Thorns Starfish on the Great Barrier Reef: Reproduction, Recruitment and Hydrodynamics. C. Johnson, ed. Aust. J. Mar. Freshwater Res. 43(3).
16. Scandol, J. P., and M. K. James. 1992. Hydrodynamics and larval dispersal: a population model of Acanthaster planci on the Great Barrier Reef. Pp. 583-596 in Crown-of-Thorns Starfish on the Great Barrier Reef: Reproduction, Recruitment and Hydrodynamics. C. Johnson, ed. Aust. J. Mar. Freshwater Res. 43(3).
17. Wolanski, E. 1993. Facts and numerical artefacts in modelling the dispersal of crown-of-thorns starfish larvae in the Great Barrier Reef. Aust. J. Mar. Freshwater Res. 44: 427-436.
18. Moran, P. J. 1986. The Acanthaster phenomenon. Oceanogr. Mar. Biol. Annu. Rev. 24: 379-480.
19. Yamaguchi, M. 1987. Occurrences and persistency of Acanthaster planci pseudo-population in relation to oceanographic conditions along the Pacific coast of Japan. Galaxea 6: 277-288.
20. DeVantier, L. M., and G. Deacon. 1990. Distribution of Acanthaster planci at Lord Howe Island, the southern-most Indo-Pacific reef. Coral Reefs 9: 145-148.
21. Benzie, J. A. H., and J. A. Stoddart. 1992. Genetic structure of crown-of-thorns starfish (Acanthaster planci) in Australia. Mar. Biol. 112: 631-639.
22. Moore, J. A. 1949. Geographaphic variation of adaptive characters in Rana pipiens Schreber. Evolution 3: 1-24.
23. Tester, P. A. 1985. Effects of parental acclimation temperature and egg-incubation temperature on egg-hatching time in Acartia tonsa (Copepoda: Calanoida). Mar. Biol. 89: 45-53.
24. Johnson, L. G. 1993. Temperature tolerance, temperature stress, and animal development. Pp. 37-40 in Proceedings of the Biostress Symposia. N. H. Granholm, ed. South Dakota State Univ., Brookings.
25. Fujisawa, H. 1989. Differences in temperature dependence of early development of sea urchins with different growing seasons. Biol. Bull. 176: 96-102.
26. O'Connor, C., and J. C. Mulley. 1977. Temperature effects on periodicity and embryology, with observations on the population genetics, of the aquacultural echinoid Heliocidaris tuberculata. Aquaculture 12: 99-114.
27. Horstadius, S. 1975. A note on the effect of temperature on sea urchin eggs. Exp. Mar. Biol. Ecol. 18: 239-242.
28. Olson, R. R. 1987. In situ culturing as a test of the larval starvation hypothesis for the crown-of-thorns starfish, Acanthaster planci. Limnol. Oceanogr. 32: 895-904.
29. Ayukai, T. 1994. Ingestion of ultraplankton by the planktonic larvae of the crown-of-thorns starfish, Acanthaster planci. Biol. Bull. 186: 90-100.
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|Author:||Johnson, Leland G.; Babcock, Russell C.|
|Publication:||The Biological Bulletin|
|Date:||Dec 1, 1994|
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