Regulation of keystone predation by small changes in ocean temperature

Science

Volumn 283, Issue 5410, 1999, Pages 2095-2097

  Sanford, Eric ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMMUNITY STRUCTURE; INTERTIDAL ENVIRONMENT; KEYSTONE SPECIES; PREDATOR; TEMPERATURE EFFECT;

ANIMAL EXPERIMENT; ARTICLE; ASTERIAS; CLIMATE; CONTROLLED STUDY; ECOSYSTEM; GEOGRAPHIC DISTRIBUTION; NONHUMAN; PREDATION; PRIORITY JOURNAL; SEA; WATER TEMPERATURE;

ANIMALIA; ASTERIAS; ASTEROIDEA; PISASTER OCHRACEUS;

EID: 0033605739     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.283.5410.2095     Document Type: Article

References (30)

1. R. L. Peters and T. E. Lovejoy, Eds., Global Warming and Biological Diversity (Yale Univ. Press, New Haven, CT, 1992); J. P. Barry, C. H. Baxter, R. D. Sagarin, S. E. Gilman, Science 267, 672 (1995); C. Parmesan, Nature 382, 765 (1996).
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6. R. T. Paine, Nature 355, 73 (1992); M. E. Power et al., Bioscience 46, 609 (1996).
7. R. T. Paine, Am. Nat. 100, 65 (1966). A similar keystone role has been demonstrated for Pisaster in Oregon [B. A. Menge, E. L. Berlow, C. A. Blanchette, S. A. Navarrete, S. B. Yamada, Ecol. Monogr. 64, 249 (1994)].
8. R. T. Paine, Am. Nat. 100, 65 (1966). A similar keystone role has been demonstrated for Pisaster in Oregon [B. A. Menge, E. L. Berlow, C. A. Blanchette, S. A. Navarrete, S. B. Yamada, Ecol. Monogr. 64, 249 (1994)].
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10. E. Sanford, unpublished data.
11. B. A. Menge et al., Proc. Natl. Acad. Sci. U.S.A. 94, 14530 (1997).
12. Replicate sites (Strawberry Hill, Pigeon Reef, and Bob Creek Wayside) were several hundred meters apart. Water temperatures generally varied < 0.2°C over these distances.
13. Mussels from a common source were transplanted under plastic Vexar mesh cages that allowed mussels to reattach to the rock and shielded them from foraging sea stars until cages were removed. Mussels reattached securely. Mean percent survivorship (± SEM) 14 days after cages were removed was 97.4 ± 0.45% on reefs without sea stars (n = 60 transplants).
14. Starting dates were set as the first day of each spring tide series.
15. Sites were inaccessible during the neap tides, days 8 through 13.
16. Temperatures recorded by the data-loggers at low tide predicted Piaster body temperature. On 20 dates, I used a digital thermometer and hypodermic probe to measure the body temperatures of 10 randomly selected sea stars at Strawberry Hill, 20 to 30 min before they were resubmerged by the incoming tide. Mean body temperature was significantly correlated with the maximum air temperature recorded by the data-logger during that low tide (y = 0.76x + 2.75, R2 = 0.85. P < 0.001).
17. E. C. Bell and M. W. Denny, J. Exp. Mar. Biol. Ecol. 181, 9 (1994).
18. o) overtime (days 1 through 14). Population interaction strengths (of) were estimated by subtracting the mean mussel survival rate (the slope of the log regression) on reefs without Pisaster from the survival rate observed in mussel transplants on reefs with Pisaster. Dividing by the mean local sea star density for that transplant and time period gave per capita interaction strength (α). This procedure gave four independent estimates of interaction strength per site x time period combination.
19. 2, n = 40).
20. I used multiple regressions to test whether variation in mean interaction strengths among time periods and sites was associated with (i) water temperature (the mean during 27 high tides per period), (ii) potential heat stress (the mean of maximum low tide air temperature on the five warmest days per period), or (iii) wave stress (the mean of maximum force per day on 5 to 7 days per period). Per capita interaction strength was associated with water temperature (P < 0.001) but was unrelated to potential heat stress (P = 0.18) or wave stress (P = 0.53). Similarly, population interaction strength was correlated with water temperature (P < 0.001) but not with potential heat stress (P = 0.13) or wave stress (P = 0.74). Site variables were significant in both models because both per capita and population interaction strength were consistently higher at Pigeon Reef, the site with higher sea star density (15). Together, water temperature and site explained 80.9% of the variation in mean per capita interaction strength and 82.4% of the variation in mean population interaction strength.
21. In early June 1996, 48 sea stars (wet weight, 118 to 138 g) were collected from Neptune State Park. Four individuals were randomly assigned to each of 12 closed 110-liter tanks held in a cold room, and heaters with controllers self-regulated treatments to ± 0.1°C. Water was circulated by two pumps in each tank, and water quality was maintained by filters and weekly water changes. Salinity was maintained at 36 ± 1 parts per thousand, and the experiments were conducted under a schedule of 12 hours of light and 12 hours of darkness. All sea stars were initially acclimated without food at 11°C for 10 days, and then treatments were randomly assigned (n = 4 tanks per treatment).
22. Mytilus trossulus was used because this species is the most common prey item in Pisaster's diet at these sites. I quantified the diet of actively feeding sea stars (n = 1664) on 14 dates during the summer of 1995 and 1996. The percents of individuals feeding on a given prey species were as follows: mussels (M. trossulus. 56.0%; M. californianus, 5.0%), barnacles (Pollicipes polymerus, 41.8%; Balanus glandula, 6.0%; Semibalanus cariousus, 3.2%; Chthamalus dalli, 1.4%; B. nubilus, 0.7%), whelks (Nucella spp., 1.5%), and limpets (Lottia spp., 0.5%). The total exceeds 100% because Pisaster often feeds on several prey species at a time.
23. Results are presented for the first three periods of the experiment. Thereafter, sea stars became temporarily satiated on the ad libitum diet, and feeding rates declined sharply in all treatments. After 4.5 months, sea stars used in the experiment had energy stores (pyloric ceca) much larger than those of field animals. Thus, the initial phase of the experiment, with sea stars recently collected from the field, best reflects the effects of temperature on Pisaster with natural levels of energy reserves.
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27. A. Bakun, Science 247, 198 (1990); D. Roemmich and J. McGowan, ibid. 267, 1324 (1995); F. B. Schwing and R. Mendelssohn, J. Geophys. Res. 102, 3421 (1997); K. E. Trenberth and T. J. Hoar, Geophys. Res. Lett. 24, 3057 (1997); J. A. McGowan, D. R. Cayan, L. M. Dorman, Science 281, 210 (1998).
28. A. Bakun, Science 247, 198 (1990); D. Roemmich and J. McGowan, ibid. 267, 1324 (1995); F. B. Schwing and R. Mendelssohn, J. Geophys. Res. 102, 3421 (1997); K. E. Trenberth and T. J. Hoar, Geophys. Res. Lett. 24, 3057 (1997); J. A. McGowan, D. R. Cayan, L. M. Dorman, Science 281, 210 (1998).
29. Pisaster ochraceus ranges from at least Punta Baja in Baja California to Prince William Sound in Alaska, and populations near these geographic limits regularly experience water temperatures >20°C and <4°C, respectively.
30. I thank L. C. Ryan for field assistance and support; P. Sanford for engineering expertise; J. Lubchenco, B. Menge, G. Allison, E. Berlow, D. Bermudez, M. Bertness, J. Burnaford, B. Grantham, P. Halpin, M. Hixon, S. Navarrete, K. Nielsen, and G. Somero for helpful discussions and reviews; and L. Weber for laboratory space at Hatfield Marine Science Center. This research was supported by a NSF Predoctoral Fellowship, the Lerner-Gray Fund for Marine Research, and a National Wildlife Federation Climate Change Fellowship, as well as NSF grants to B. Menge and funds provided to J. Lubchenco and B. Menge by the Andrew W. Mellon and Wayne & Gladys Valley Foundations.