Expanded consumer niche widths may signal an early response to spatial protection

English version

Autoři: Angeleen M. Olson ^aff001; Rowan Trebilco ^aff001; Anne K. Salomon ^aff001
Působiště autorů: School of Resource and Environmental Management, Simon Fraser University, Faculty of Science, Burnaby, British Columbia, Canada ^aff001; Hakai Institute, Heriot Bay, British Columbia, Canada ^aff002; Antarctic Climate and Ecosystems CRC, University of Tasmania, Hobart, Tasmania, Australia ^aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223748

Souhrn

Marine management interventions are increasingly being implemented with the explicit goal of rebuilding ocean ecosystems, but early responses may begin with alterations in ecological interactions preceding detectable changes in population-level characteristics. To establish a baseline from which to monitor the effects of spatial protection on reef fish trophic ecology and track future ecosystem-level changes, we quantified temperate reef fish densities, size, biomass, diets and isotopic signatures at nine sites nested within two fished and one five-year old marine protected area (MPA) on the northwest coast of Canada. We calculated rockfish (Sebastes spp.) community and species-specific niche breadth for fished and protected areas based on δ¹³C and δ¹⁵N values. We found that rockfish community niche width was greater inside the MPA relative to adjacent fished reefs due to an expanded nitrogen range, possibly reflecting early changes in trophic interactions following five years of spatial protection. Our data also demonstrated that the MPA had a positive effect on the δ¹⁵N signature of rockfish (i.e., trophic position), but the effect of rockfish length on its own was not well-supported. In addition, we found a positive interaction between rockfish length and δ¹⁵N signature, such that δ¹⁵N signatures of rockfish caught within the MPA increased more rapidly with body size than those caught in fished areas. Differences in rockfish size structure and biomass among fished and unfished areas were not clearly evident. Species of rockfish and lingcod varied in trophic and size responses, indicating that life-history traits play an important role in predicting MPA effects. These results may suggest early changes in trophic behavior of slow-growing rockfish due to predation risk by faster growing higher trophic level predators such as lingcod inside MPAs established on temperate reefs. Consequently, spatial protection may restore both the trophic and behavioral roles of previously fished consumers earlier and in measurable ways sooner than observable changes in abundance and size.

Klíčová slova:

Reefs – Trophic interactions – Predation – Ecological niches – Conservation science – Marine fish – Food web structure – Marine ecosystems

Zdroje

1. Mangel M, Levin PS. Regime, phase and paradigm shifts: making community ecology the basic science for fisheries. Philos Trans R Soc Lond, B. 2005;360: 95–105.

2. Lindenmayer DB, Franklin JF, Lõhmus A, Baker SC, Bauhus J, Beese W, et al. A major shift to the retention approach for forestry can help resolve some global forest sustainability issues. Conserv Lett. 2012;5: 421–431.

3. Messier C, Puettmann K, Chazdon R, Andersson KP, Angers VA, Brotons L, et al. From management to stewardship: Viewing forests as complex adaptive systems in an uncertain world. Conserv Lett. 2015;8: 368–377.

4. Pikitch EK, Santora C, Babcock EA, Bakun A, Bonfil R, Conover DO, et al. Ecosystem-based fishery management. Science. 2004;305: 346–347. doi: 10.1126/science.1098222 15256658

5. Meadows DH. Thinking in Systems. Wright D, editor. Chelsea Green Publishing; 2008.

6. Link J. What does ecosystem-based fisheries management mean. Fisheries. 2002;27: 18–21.

7. Smith ADM, Fulton EJ, Hobday AJ, Smith DC, Shoulder P. Scientific tools to support the practical implementation of ecosystem-based fisheries management. ICES J Mar Sci. 2007;64: 633–639.

8. Levin PS, Fogarty MJ, Murawski SA, Fluharty D. Integrated ecosystem assessments: developing the scientific basis for ecosystem-based management of the ocean. PLoS Biol. 2009;7: e1000014.

9. Elton CS. Animal ecology, by Charles Elton; with an introduction by Julian S. Huxley. New York,: Macmillan Co; 1927.

10. Hutchinson GE. Concluding Remarks. Cold Spring Harbor Symposia on Quantitative Biology. Cold Spring Harbor Laboratory Press; 1957;22: 415–427.

11. Leibold MA. The niche concept revisited: Mechanistic models and community context. Ecology. 1995;76: 1371–1382.

12. Newsome SD, del Rio CM, Bearhop S, Phillips DL. A niche for isotopic ecology. Front Ecol Environ. 2007;5: 429–436.

13. Layman CA, Arrington DA, Montaña CG, Post DM. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology. 2007;88: 42–48. doi: 10.1890/0012-9658(2007)88[42:csirpf]2.0.co;2 17489452

14. Salomon AK, Waller NP, McIlhagga C, Yung RL, Walters C. Modeling the trophic effects of marine protected area zoning policies: A case study. Aquat Ecol. 2002;36: 85–95.

15. Baskett ML, Micheli F, Levin SA. Designing marine reserves for interacting species: Insights from theory. Biol Conserv. 2007;137: 163–179.

16. White JW, Botsford LW, Baskett ML, Barnett LA, Barr RJ, Hastings A. Linking models with monitoring data for assessing performance of no‐take marine reserves. Front Ecol Environ. 2011;9: 390–399.

17. Babcock RC, Kelly S, Shears NT, Walker JW, Willis TJ. Changes in community structure in temperate marine reserves. Mar Ecol Prog Ser. 1999;189: 125–134.

18. McClanahan TR. Predation and the control of the sea urchin Echinometra viridis and fleshy algae in the patch reefs of Glovers Reef, Belize. Ecosystems. 1999;2: 511–523.

19. Shears NT, Babcock RC. Marine reserves demonstrate top-down control of community structure on temperate reefs. Oecologia. 2002;132: 131–142. doi: 10.1007/s00442-002-0920-x 28547276

20. Salomon AK, Shears NT, Langlois TJ, Babcock RC. Cascading effects of fishing can alter carbon flow through a temperate coastal ecosystem. Ecol Appl. 2008;18: 1874–1887. doi: 10.1890/07-1777.1 19263885

21. Hamilton SL, Newsome SD, Caselle JE. Dietary niche expansion of a kelp forest predator recovering from intense commercial exploitation. Ecology. 2014;95: 164–172. doi: 10.1890/13-0014.1 24649656

22. Shears NT, Babcock RC, Salomon AK. Context-dependent effects of fishing: variation in trophic cascades across environmental gradients. Ecol Appl. 2008;18: 1860–1873. doi: 10.1890/07-1776.1 19263884

23. Salomon AK, Gaichas SK, Shears NT, Smith JE, Madin EMP, Gaines SD. Key features and context‐dependence of fishery‐induced trophic cascades. Conserv Biol. 2010;24: 382–394. doi: 10.1111/j.1523-1739.2009.01436.x 20151987

24. Babcock RC, Shears NT, Alcala AC, Barrett NS, Edgar GJ, Lafferty KD, et al. Decadal trends in marine reserves reveal differential rates of change in direct and indirect effects. Proc Natl Acad Sci. 2010;107: 18256–18261. doi: 10.1073/pnas.0908012107 20176941

25. Claudet J, Osenberg CW, Domenici P, Badalamenti F, Milazzo M, Falcón JM, et al. Marine reserves: fish life history and ecological traits matter. Ecol Appl. 2010;20: 830–839. doi: 10.1890/08-2131.1 20437967

26. Russ GR, Alcala AC. Effects of intense fishing pressure on an assemblage of coral reef fishes. Mar Ecol Prog Ser. 1989;56: 13–27.

27. Denny CM, Willis TJ, Babcock RC. Rapid recolonisation of snapper Pagrus auratus: Sparidae within an offshore island marine reserve after implementation of no-take status. Mar Ecol Prog Ser. 2004;272: 183–190.

28. Love MS, Yoklavich M, Thorsteinson LK. The rockfishes of the Northeast Pacific. Univ of California Press; 2002.

29. DFO. Straight of Georgia Lingcod (Ophiodon elongatus) Assessment and advise for fishery management. 2005.

30. Yamanaka KL, Logan G. Developing British Columbia's Inshore Rockfish Conservation Strategy. Mar Coast Fish. 2010;2: 28–46.

31. Brady C, Thom BA, Matson S, Seekins B, Hanshew G, Couch R, et al. Trawl Rockfish Conservation Area (RCA) boundary modifications: final environmental assessment. NOAA. 2014.

32. Beaudreau AH, Essington TE. Spatial, temporal, and ontogenetic patterns of predation on rockfishes by lingcod. T Am Fish Soc. 2007;136: 1438–1452.

33. Hamel OS, Sethi SA, Wadsworth TF. Status and future prospects for lingcod in waters off Washington, Oregon, and California as assessed in 2009. Status of the Pacific coast groundfish fishery through. 2009.

34. Oken KL, Essington TE. Evaluating the effect of a selective piscivore fishery on rockfish recovery within marine protected areas. ICES J Mar Sci. 2016;73: 2267–2277.

35. Frid A, McGreer M, Haggarty DR, Beaumont J, Gregr EJ. Rockfish size and age: The crossroads of spatial protection, central place fisheries and indigenous rights. Glob Ecol Conserv. 2016;8: 170–182.

36. Brown CJ, Trebilco R. Unintended cultivation, shifting baselines, and conflict between objectives for fisheries and conservation. Conserv Biol. 2014;28: 677–688. doi: 10.1111/cobi.12267 24665891

37. Trebilco R, Demes KW, Lee LC, Keeling BE, Sloan NA, Stewart HL, et al. Summary of baseline kelp forest surveys within and adjacent to Gwaii Haanas National Park Reserve, National Marine Conservation Area Reserve and Haida Heritage Site, Haida Gwaii, British Columbia, Canada. 2014.

38. Canada Parks. Living marine legacy of Gwaii Haanas. V: Coastal zone values and management around Haida Gwaii. Sloan NA, editor. Parks Canada Technical Reports in Ecosystem Science. 2006 Dec pp. 1–446.

39. Canada Parks. Gwaii Haanas Gina ‘Waadluxan KilGuhlGa Land-Sea People Management Plan. Council of the Haida Nation and Her Majesty the Queen in Right of Canada, represented by the Chief Executive Officer of Parks Canada; 2018 Nov.

40. Shears NT, Babcock RC. Continuing trophic cascade effects after 25 years of no-take marine reserve protection. Mar Ecol Prog Ser. 2003;246: 1–16.

41. Edgar GJ, Stuart-Smith RD, Willis TJ, Kininmonth S, Baker SC, Banks S, et al. Global conservation outcomes depend on marine protected areas with five key features. Nature. 2014;506: 216–220. doi: 10.1038/nature13022 24499817

42. Froese R, Pauly D. FishBase [Internet]. 2012. Available: www.fishbase.org

43. Levin LA, Currin C. Stable isotope protocols: Sampling and sample processing. 2012.

44. Jackson AL, Inger R, Parnell AC, Bearhop S. Comparing isotopic niche widths among and within communities: SIBER—Stable Isotope Bayesian Ellipses in R. J Anim Ecol. 2011;80: 595–602. doi: 10.1111/j.1365-2656.2011.01806.x 21401589

45. Parnell AC, Jackson AL. SIAR: Stable Isotope Analysis in R. 2011 pp. 1–34.

46. Inman HF, Bradley EL Jr. The overlapping coefficient as a measure of agreement between probability distributions and point estimation of the overlap of two normal densities. Commun Stat-Theor M. 1989;18: 3851–3874.

47. Bates D, Maechler M, Bolker B, Walker S. lme4: Linear mixed-effects models using Eigen and S4. R package version 1.7. 2014

48. Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM. Mixed effects models and extensions in ecology with R. New York, NY: Springer New York; 2009.

49. Jennings S, Barnes C, Sweeting CJ, Polunin NVC. Application of nitrogen stable isotope analysis in size-based marine food web and macroecological research. Rapid Commun Mass Spectrom. 2008;22: 1673–1680. doi: 10.1002/rcm.3497 18438766

50. Burnham KP, Anderson DR. Model Selection and Inference. New York, NY: Springer Science & Business Media; 2013.

51. Barton K. MuMIn: R package for multi-model inference. Version 1.40.4. 2018.

52. Gelman A. Scaling regression inputs by dividing by two standard deviations. Stat Med. 2008;27: 2865–2873. doi: 10.1002/sim.3107 17960576

53. Behrens MD, Lafferty KD. Effects of marine reserves and urchin disease on southern Californian rocky reef communities. Mar Ecol Prog Ser. 2004;279: 129–139.

54. Micheli F, Benedetti-Cecchi L, Gambaccini S, Bertocci I, Borsini C, Osio GC, et al. Cascading human impacts, marine protected areas, and the structure of Mediterranean reef assemblages. Ecol Monogr. 2005;75: 81–102.

55. Selden RL, Gaines SD, Hamilton SL, Warner RR. Protection of large predators in a marine reserve alters size-dependent prey mortality. Proc R Soc B. 2017;284: 20161936. doi: 10.1098/rspb.2016.1936 28123086

56. Dell C, Montoya JP, Hay ME. Effect of marine protected areas (MPAs) on consumer diet: MPA fish feed higher in the food chain. Mar Ecol Prog Ser. 2015;540: 227–234. doi: 10.3354/meps11487 27340314

57. Davis JP, Valle CF, Haggerty MB, Walker K, Gliniak HL, Van Diggelen AD, et al. Testing trophic indicators of fishery health in California’s marine protected areas for a generalist carnivore. Ecol Indic. 2018;97: 419–428.

58. Frid A, Marliave J, Heithaus MR. Interspecific variation in life history relates to antipredator decisions by marine mesopredators on temperate reefs. Boyce MS, editor. PLoS ONE. 2012;7: e40083. doi: 10.1371/journal.pone.0040083 22768226

59. Frid A, Connors B, Cooper AB, Marliave J. Size-structured abundance relationships between upper- and mid-trophic level predators on temperate rocky reefs. Ethol Ecol Evol. 2013;25: 253–268.

60. Cass AJ, Beamish RJ, McFarlane GA. Lingcod (Ophiodon elongatus). Can Spec Pub Fish Aquat Sci. 1990;109: 1–47.

61. Johnson K. Status Report: Census of lingcod nesting activity in the Edmonds Underwater Park. In 2003 Georgia Basin/Puget Sound Research Conference Proceedings. Feb 2004.

62. Martell SJD, Walters CJ, Wallace SS. The use of marine protected areas for conservation of lingcod (Ophiodon elongatus). Bull Mar Sci. 2000;66: 729–743.

63. Beaudreau AH, Essington TE. Development of a new field-based approach for estimating consumption rates of fishes and comparison with a bioenergetics model for lingcod (Ophiodon elongatus). Can J Fish Aquat Sci. 2009;66: 565–578.

64. Oken KL, Essington TE. Evaluating the effect of a selective piscivore fishery on rockfish recovery within marine protected areas. ICES J Mar Sci. 2016;73: 2267–2277.

65. Dill LM, Heithaus MR, Walters CJ. Behaviorally mediated indirect interactions in marine communities and their conservation implications. Ecology. 2003;84: 1151–1157.

66. Walters CJ, Juanes F. Recruitment limitation as a consequence of natural selection for use of restricted feeding habitats and predation risk taking by juvenile fishes. Can J Fish Aquat Sci. 1993;50: 2058–2070.

67. Skilleter GA, Peterson CH. Control of foraging behavior of individuals within an ecosystem context: the clam Macoma balthica and interactions between competition and siphon cropping. Oecologia. 1994;100: 268–278. doi: 10.1007/BF00316954 28307010

68. Markel RW, Shurin JB. Indirect effects of sea otters on rockfish (Sebastes spp.) in giant kelp forests. Ecology. 2015;96: 2877–2890. doi: 10.1890/14-0492.1 27070008

69. Trebilco R, Dulvy NK, Anderson SC, Salomon AK. The paradox of inverted biomass pyramids in kelp forest fish communities. Proc R Soc B. 2016;283: 20160816. doi: 10.1098/rspb.2016.0816 27335422

70. Jabot F, Giraldo C, Lefebvre S, Dubois S. Are food web structures well represented in isotopic spaces? Funct Ecol. 2017;31: 1975–1984.

71. Sinopoli M, Fanelli E, D’Anna G, Badalamenti F, Pipitone C. Assessing the effects of a trawling ban on diet and trophic level of hake, Merluccius merluccius, in the southern Tyrrhenian Sea. Sci Mar. 2012;0: 1–14.

72. Loury EK, Bros SM, Starr RM, Ebert DA, Cailliet GM. Trophic ecology of the gopher rockfish Sebastes carnatus inside and outside of central California marine protected areas. Mar Ecol Prog Ser. 2015;536: 229–241.

73. Baskett ML, Micheli F, Levin SA. Designing marine reserves for interacting species: Insights from theory. Biol Conserv. 2007;137: 163–179.

74. Lafferty KD. Fishing for lobsters indirectly increases epidemics in sea urchins. Ecol Appl. 2004;14: 1566–1573.

75. Trebilco R, Dulvy NK, Stewart H, Salomon AK. The role of habitat complexity in shaping the size structure of a temperate reef fish community. Mar Ecol Prog Ser. 2015;532: 197–211.

Expanded consumer niche widths may signal an early response to spatial protection

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz