Synergistic predation, density dependence, and population regulation in marine fish

Science

Volumn 277, Issue 5328, 1997, Pages 946-949

  Hixon, Mark A ^a   Carr, Mark H ^b  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DENSITY DEPENDENCE; POPULATION REGULATION; PREDATION; PREDATOR-PREY INTERACTION; REEF FISH;

ARTICLE; FISH; MORTALITY; NONHUMAN; POPULATION DENSITY; POPULATION DYNAMICS; PREDATION; PRIORITY JOURNAL;

CHROMIS CYANEA;

EID: 0030848021     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.277.5328.946     Document Type: Article

References (54)

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18. H. W. van der Veer, Mar. Ecol. Prog. Ser. 29, 223 (1986); S. Sundby, H. Bjorke, A. V. Soldal, S. Olsen, Rapp. P-V. Reun. Cons. Int. Explor. Mer. 191, 351 (1989); R. A. Myers and N. G. Cadigan, Can. J. Fish. Aquat. Sci. 50, 1576 (1993); K. M. Bailey, Neth. J. Sea Res. 32, 175 (1994). Note that "births" in local populations of demersal marine fish are usually by the process of dispersive pelagic larvae settling to the bottom. By manipulating the density of settling larvae, one could essentially control local births to test for density dependence in subsequent mortality.
19. H. W. van der Veer, Mar. Ecol. Prog. Ser. 29, 223 (1986); S. Sundby, H. Bjorke, A. V. Soldal, S. Olsen, Rapp. P-V. Reun. Cons. Int. Explor. Mer. 191, 351 (1989); R. A. Myers and N. G. Cadigan, Can. J. Fish. Aquat. Sci. 50, 1576 (1993); K. M. Bailey, Neth. J. Sea Res. 32, 175 (1994). Note that "births" in local populations of demersal marine fish are usually by the process of dispersive pelagic larvae settling to the bottom. By manipulating the density of settling larvae, one could essentially control local births to test for density dependence in subsequent mortality.
20. H. W. van der Veer, Mar. Ecol. Prog. Ser. 29, 223 (1986); S. Sundby, H. Bjorke, A. V. Soldal, S. Olsen, Rapp. P-V. Reun. Cons. Int. Explor. Mer. 191, 351 (1989); R. A. Myers and N. G. Cadigan, Can. J. Fish. Aquat. Sci. 50, 1576 (1993); K. M. Bailey, Neth. J. Sea Res. 32, 175 (1994). Note that "births" in local populations of demersal marine fish are usually by the process of dispersive pelagic larvae settling to the bottom. By manipulating the density of settling larvae, one could essentially control local births to test for density dependence in subsequent mortality.
21. M. P. Sissenwine, in Exploitation of Marine Communities, R. M. May, Ed. (Springer-Verlag, Berlin, Germany, 1984), pp. 59-94.
22. M. H. Carr and M. A. Hixon, Mar. Ecol. Prog. Ser. 124, 31 (1995); unpublished data.
23. Resident predators in the Bahamian system, some of which forage at night, include moray eels (especially Gymnothorax moringa), large squirrelfishes (especially Holocentrus ascensionis), and some snapper (Lutjanus spp.), but mostly grouper (especially Epinephelus striatus). Transient predators include rare lizardfishes (Synodus spp.) and a snapper (Lutjanus synagris), but by far, mostly jacks (particularly Caranx ruber). Unlike its predators, C. cyanea is not fished by humans.
24. B. A. de Boer, Bull. Mar. Sci. 28, 550 (1978).
25. 2 in area, certainly a realistic spatial scale for this system [see (3) and (6) for discussion].
26. A. Sih et al., Annu. Rev. Ecol. Syst. 16, 269 (1985).
27. M. A. Hixon, in The Ecology of Fishes on Coral Reefs, P. F. Sale, Ed. (Academic Press, San Diego, CA, 1991), pp. 475-508.
28. Translocated reefs, each averaging 11 coral heads 30 to >100 cm in diameter, grew on loose rubble and so did not have to be broken off the bottom. The coral heads were moved unharmed underwater on the central elevator platform of a specially designed motorized catamaran (10). Through the summer of 1996, the corals had survived well in their new locations. Translocated reefs used in each experiment had been recolonized by fishes to natural densities.
29. Natural isolation distances of patch reefs in this region range broadly, up to several kilometers.
30. Drifter studies by B. Hickey and E. Elliott (University of Washington) showed that tidal-current water that brings settlement-competent larvae to our experimental reefs first passes over several kilometers of shallow fore-reef, giving larvae ample opportunity to settle before arriving at our experimental reefs.
31. In 1996, we microtagged and transplanted 20 new settlers of Chromis to each of four translocated reefs similar to the experimental reefs, but isolated by only 100 m from each other and nearby unmanipulated reefs. Over the next month, these fish disappeared at a per capita rate (mean ± SEM = 0.44 ± 0.10) comparable with that on experimental reefs exposed to predation (Fig. 2A). Importantly, despite 10 exhaustive searches over the month of all reefs within 200 m of the release sites, none of the missing tagged fish appeared on any neighboring reef, substantiating that disappearance in this system is tantamount to mortality. Moreover, even on continuous fore-reefs, of 95 new settlers microtagged in seven distinct social groups and followed for a month, only one fish emigrated successfully (to a group only 5 m away). For microtagging methods, see R. M. Buckley, J. E. West, D. C. Doty, Bull. Mar. Sci. 55, 848 (1994); J. S. Beukers, G. P. Jones, R. M. Buckley, Mar. Ecol. Prog. Ser. 125, 61 (1995).
32. In 1996, we microtagged and transplanted 20 new settlers of Chromis to each of four translocated reefs similar to the experimental reefs, but isolated by only 100 m from each other and nearby unmanipulated reefs. Over the next month, these fish disappeared at a per capita rate (mean ± SEM = 0.44 ± 0.10) comparable with that on experimental reefs exposed to predation (Fig. 2A). Importantly, despite 10 exhaustive searches over the month of all reefs within 200 m of the release sites, none of the missing tagged fish appeared on any neighboring reef, substantiating that disappearance in this system is tantamount to mortality. Moreover, even on continuous fore-reefs, of 95 new settlers microtagged in seven distinct social groups and followed for a month, only one fish emigrated successfully (to a group only 5 m away). For microtagging methods, see R. M. Buckley, J. E. West, D. C. Doty, Bull. Mar. Sci. 55, 848 (1994); J. S. Beukers, G. P. Jones, R. M. Buckley, Mar. Ecol. Prog. Ser. 125, 61 (1995).
33. For piscivore manipulations, resident predators were captured unharmed by divers with hand nets, tagged, and released at least 2 km from the study site. Transient predators were excluded from reefs by large cages (21). For Chromis manipulations, numbers of larger fish on experimental reefs were first adjusted to a narrow natural range (two to four fish per reef). New settlers, identified by their small size (<2 cm total length) and partial pigmentation (mostly gray in appearance), were then captured on the fore-reef with BINCKE nets (T. W. Anderson and M. H. Carr, Env. Biol. Fish., in press), placed in plastic bags of seawater in situ for transport, and released on experimental reefs to attain desired densities for at least 24 hours before the start of an experiment. To test whether this transplant method artificially increased Chromis mortality, we compared, in separate but complementary experiments each year, per capita mortality among three treatments: (i) groups of uncaptured fish, (ii) groups of fish captured and returned to the same location after being transported halfway to experimental reefs and back, and (iii) groups of fish experimentally transplanted to new reefs. Analysis of variance of these treatments indicated no deleterious effects of handling or transplanting (10).
34. Circular reef-enclosure cages, constructed of 1.5-cm nylon mesh, were 6 m in diameter and extended from the surface to the bottom (3 to 4 m deep). They were attached to the bottom by earth anchors, sealed by heavy chain, and supported by floats. Although impermeable to larger fish, the cages were transparent to movements of newly settled Chromis and other small fishes. Partial control cages consisted of four net panels interdigitated with four open panels so that transient predators could enter.
35. For related examples of the regression approach, see G. E. Forrester, Oecologia 103, 275 (1995); M. A. Steele, Ecology 78, 129 (1997).
36. For related examples of the regression approach, see G. E. Forrester, Oecologia 103, 275 (1995); M. A. Steele, Ecology 78, 129 (1997).
37. The fact that the y intercepts of the mortality curves (an estimate of the underlying density-independent mortality rate) were nearly identical for caged reefs lacking all predators (0.275, Fig. 2D) and uncaged reefs exposed to all predators (0.309, Fig. 2A), is further evidence that the reef enclosures did not artificially affect the background mortality of the study fish. Note also that mortality rates from the experiment in 1995 (as well as previous years) were similar to those in 1996 (Fig. 2), lending credence to the temporal generality of our results. Analysis of instantaneous per capita mortality rates revealed that the major period of density dependence occurred during the first 5 days of the experiment.
38. W. W. Murdoch and A. Oaten, Adv. Ecol. Res. 9, 1 (1975).
39. W. W. Murdoch and J. Bence, in Predation: Direct and Indirect Impacts on Aquatic Communities, W. C. Kerfoot and A. Sih, Eds. (Univ. Press of New England, Hannover, NH, 1987), pp. 17-30.
40. M. P. Hassell and R. M. May, J. Anim. Ecol. 43, 567 (1974).
41. M. A. Hixon and J. P. Beets, Ecol. Monogr. 63, 77 (1993).
42. As detailed elsewhere (10), we placed two Hi-8 video camera units underwater such that each viewed an entire experimental reef from the side, recording 15 s out of every 90 s from dawn to dusk. On 13 dates during the 1996 experiment, we conducted paired video samples of uncaged reefs with low (mean ± SEM = 5.4 ± 0.4 fish per reef) versus high (20.4 ± 1.7 fish per reef) experimental densities of newly settled Chromis.
43. We do not believe that this discrepancy could be due to nonbehavioral mechanisms, such as variable resident predator density. The densities of resident piscivores were unmanipulated in the two treatments where this suite of predators was present, so there was indeed natural variation among reefs in resident predator density. However, there was no significant difference in resident predator density between the treatment where all predators were present (mean ± SEM = 9.8 ± 1.3 fish per reef) and the treatment where only resident predators were present (11.0 ± 2.7 fish per reef, Mann-Whitney U-test, P = 0.88, n = 8 reefs each). Also, there was no correlation among reefs within either treatment between the density of resident piscivores and per capita settler mortality (correlation coefficient, r, = -0.21, P = 0.61 and r = -0.42, P = 0.31, respectively).
44. A. C. Hurley and P. H. Hartline, Anim. Behav. 22, 430 (1974); E. S. Hobson and J. R. Chess, Fish. Bull. 76, 133 (1978); M. Hixon and M. Carr, personal observation.
45. A. C. Hurley and P. H. Hartline, Anim. Behav. 22, 430 (1974); E. S. Hobson and J. R. Chess, Fish. Bull. 76, 133 (1978); M. Hixon and M. Carr, personal observation.
46. A. C. Hurley and P. H. Hartline, Anim. Behav. 22, 430 (1974); E. S. Hobson and J. R. Chess, Fish. Bull. 76, 133 (1978); M. Hixon and M. Carr, personal observation.
47. W. P. Davis and R. S. Birdsong, Helgo. Wiss. Meeresunters. 24, 292 (1973); P. G. Sackley and L. S. Kaufman, Copeia 1996, 726 (1996). Midwater is safe for small fishes because resident predators tend to stay in cover, being prey of very large transient predators, especially great barracuda (Sphyraena barracuda) at our study site. We often observed barracuda attacking and capturing resident piscivores, and barracuda tooth scars were common on these fish. Barracuda ignored new settlers.
48. W. P. Davis and R. S. Birdsong, Helgo. Wiss. Meeresunters. 24, 292 (1973); P. G. Sackley and L. S. Kaufman, Copeia 1996, 726 (1996). Midwater is safe for small fishes because resident predators tend to stay in cover, being prey of very large transient predators, especially great barracuda (Sphyraena barracuda) at our study site. We often observed barracuda attacking and capturing resident piscivores, and barracuda tooth scars were common on these fish. Barracuda ignored new settlers.
49. P. J. Doherty and T. Fowler, Science 263, 935 (1994).
50. W. J. Richards and J. A. Bohnsack, in Large Marine Ecosystems: Patterns, Processes, and Yields, K. Sherman, L. M. Alexander, B. D. Gold, Eds. (American Association for the Advancement of Science, Washington, DC, 1990), pp. 44-53; G. R. Russ, in The Ecology of Fishes on Coral Reefs, P. F. Sale, Ed. (Academic Press, San Diego, CA, 1991), pp. 601-635; S. Jennings and J. M. Lock, in Reef Fisheries, N. V. C. Polunin and C. M. Roberts, Eds. (Chapman & Hall, London, UK, 1996), pp. 193-218.
51. W. J. Richards and J. A. Bohnsack, in Large Marine Ecosystems: Patterns, Processes, and Yields, K. Sherman, L. M. Alexander, B. D. Gold, Eds. (American Association for the Advancement of Science, Washington, DC, 1990), pp. 44-53; G. R. Russ, in The Ecology of Fishes on Coral Reefs, P. F. Sale, Ed. (Academic Press, San Diego, CA, 1991), pp. 601-635; S. Jennings and J. M. Lock, in Reef Fisheries, N. V. C. Polunin and C. M. Roberts, Eds. (Chapman & Hall, London, UK, 1996), pp. 193-218.
52. W. J. Richards and J. A. Bohnsack, in Large Marine Ecosystems: Patterns, Processes, and Yields, K. Sherman, L. M. Alexander, B. D. Gold, Eds. (American Association for the Advancement of Science, Washington, DC, 1990), pp. 44-53; G. R. Russ, in The Ecology of Fishes on Coral Reefs, P. F. Sale, Ed. (Academic Press, San Diego, CA, 1991), pp. 601-635; S. Jennings and J. M. Lock, in Reef Fisheries, N. V. C. Polunin and C. M. Roberts, Eds. (Chapman & Hall, London, UK, 1996), pp. 193-218.
53. S. L. Pimm and J. B. Hyman, Can. J. Fish. Aquat. Sci. 44, 84 (1987).
54. For backbreaking work, we thank G. Almany, T. Anderson, J. Beets, R. Buckley. M. Buckley, B. Byrne, D. Canestro, G. Forrester, R. Gomez, A. Kaltenberg, A. Menge, G. Savage, S. Thompson, C. Tinus, E. Tynes, K. Vicknair, and M. Webster, and for general support, the staff of the Caribbean Marine Research Center, especially C. Cooper, G. Dennis, W. Head, W. Keith-Hardy, R. Wicklund, and T. Wolcott. Thanks to G. Almany, T. Anderson, K. Bailey, P. Bailey, J. Beets, C. Briggs, B. Byrne, J. Lubchenco, D. Reed, W. Pearcy, S. Sogard, and M. Webster for constructive reviews. Supported by NSF (OCE-92-17163 and OCE-96-17483) and National Oceanic and Atmospheric Administration's National Undersea Research Program (CMRC-92-46, 93-12, 94-15, 95-3042, and 97-3109).