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Predators reverse the direction of density dependence for juvenile salmon mortality

  • Population Ecology - Original Paper
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Abstract

The effect of predators on prey populations depends on how predator-caused mortality changes with prey population density. Predators can enforce density-dependent prey mortality and contribute to population stability, but only if they have a positive numerical or behavioral response to increased prey density. Otherwise, predator saturation can result in inversely density-dependent mortality, destabilizing prey populations and increasing extinction risk. Juvenile salmon and trout provide some of the clearest empirical examples of density-dependent mortality in animal populations. However, although juvenile salmon are very vulnerable to predators, the demographic effects of predators on juvenile salmon are unknown. We tested the interactive effects of predators and population density on the mortality of juvenile Atlantic salmon (Salmo salar) using controlled releases of salmon in natural streams. We introduced newly hatched juvenile salmon at three population density treatments in six study streams, half of which contained slimy sculpin (Cottus cognatus), a common generalist predator (18 release sites in total, repeated over two summers). Sculpin reversed the direction of density dependence for juvenile salmon mortality. Salmon mortality was density dependent in streams with no sculpin, but inversely density dependent in streams where sculpin were abundant. Such predator-mediated inverse density dependence is especially problematic for prey populations suppressed by other factors, thereby presenting a fundamental challenge to persistence of rare populations and restoration of extirpated populations.

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References

  • Anderson TW (2001) Predator responses, prey refuges, and density-dependent mortality of a marine fish. Ecology 82:245–257

    Article  Google Scholar 

  • Armstrong JD (2005) Spatial variation in population dynamics of juvenile Atlantic salmon: implications for conservation and management. J Fish Biol 67[Suppl B]:35–52

    Article  Google Scholar 

  • Baker JP et al (1996) Episodic acidification of small streams in the northeastern United States: effects on fish populations. Ecol Appl 6:422–437

    Article  Google Scholar 

  • Beall E, Dumas J, Claireaux D, Barriere L, Marty C (1994) Dispersal patterns and survival of Atlantic salmon (Salmo salar) juveniles in a nursery stream. ICES J Mar Sci 51:1–9

    Article  Google Scholar 

  • Benke AC, Huryn AD, Smock LA, Wallace JB (1999) Length–mass relationships for freshwater macroinvertebrates in North America with particular reference to the southeastern United States. J North Am Benthol Soc 18:308–343

    Article  Google Scholar 

  • Berejikian BA (1995) The effects of hatchery and wild ancestry and experience on the relative ability of steelhead trout fry (Oncorhynchus mykiss) to avoid a benthic predator. Can J Fish Aquat Sci 52:2476–2482

    Google Scholar 

  • Brannas E (1995) First access to territorial space and exposure to strong predation pressure: a conflict in early emerging Atlantic Salmon (Salmo salar L.) fry. Evol Ecol 9:411–420

    Article  Google Scholar 

  • Carle FL, Strub MR (1978) A new method for estimating population size from removal data. Biometrics 34:621–830

    Article  Google Scholar 

  • de Gaudemar B, Schroder SL, Beall EP (2000) Nest placement and egg distribution in Atlantic salmon redds. Environ Biol Fishes 57:37–47

    Article  Google Scholar 

  • Egglishaw HJ, Shackley PE (1977) Growth, survival and production of juvenile salmon and trout in a Scottish stream, 1966–75. J Fish Biol 11:647–672

    Article  Google Scholar 

  • Einum S, Nislow KH (2005) Local-scale density-dependent survival of mobile organisms in continuous habitats: an experimental test using Atlantic salmon. Oecologia 143:203–210

    Article  PubMed  Google Scholar 

  • Elliott JM (1994) Quantitative ecology and the brown trout. Oxford University Press, Oxford

    Google Scholar 

  • Elliott JM (2006) Periodic habitat loss alters the competitive coexistence between brown trout and bullheads in a small stream over 34 years. J Anim Ecol 75:54–63

    Article  PubMed  CAS  Google Scholar 

  • Folt CL, Burns CW (1999) Biological drivers of zooplankton patchiness. Trends Ecol Evol 14:300–305

    Article  PubMed  Google Scholar 

  • Folt CL, Nislow KH, Power ME (1998) Implications of temporal and spatial scale for Atlantic salmon (Salmo salar) research. Can J Fish Aquat Sci 55:9–21

    Article  Google Scholar 

  • Foote CJ, Brown GS (1998) Ecological relationship between freshwater sculpins (genus Cottus) and beach-spawning sockeye salmon (Oncorhynchus nerka) in Iliamna Lake, Alaska. Can J Fish Aquat Sci 55:1524–1533

    Article  Google Scholar 

  • Gascoigne JC, Lipcius RN (2004) Allee effects driven by predation. J Appl Ecol 41:801–810

    Article  Google Scholar 

  • Gaudin P, Caillere L (2000) Experimental study of the influence of presence and predation by sculpin, Cottus gobio L., on the drift of emergent brown trout, Salmo trutta L. Arch Hydrobiol 147:257–271

    Google Scholar 

  • Gephard S, McMenemy JR (2004) An overview of the program to restore Atlantic salmon and other diadromous fishes to the Connecticut River with notes on the current status of these species in the river. Am Fish Soc Monogr 9:287–317

    Google Scholar 

  • Ginzburg LR, Ferson S, Akcakaya HR (1990) Reconstructibility of density dependence and the conservative assessment of extinction risks. Conserv Biol 4:63–70

    Article  Google Scholar 

  • Gray MA, Cunjak RA, Munkittrick KR (2004) Site fidelity of slimy sculpin (Cottus cognatus): insights from stable carbon and nitrogen analysis. Can J Fish Aquat Sci 61:1717–1722

    Article  Google Scholar 

  • Henderson JN, Letcher BH (2003) Predation on stocked Atlantic salmon (Salmo salar) fry. Can J Fish Aquat Sci 60:32–42

    Article  Google Scholar 

  • Hixon MA, Carr MH (1997) Synergistic predation, density dependence, and population regulation in marine fish. Science 277:946–949

    Article  CAS  Google Scholar 

  • Hixon MA, Jones GP (2005) Competition, predation, and density-dependent mortality in demersal marine fishes. Ecology 86:2847–2859

    Article  Google Scholar 

  • Hixon MA, Pacala SW, Sandin SA (2002) Population regulation: historical context and contemporary challenges of open vs. closed systems. Ecology 83:1490–1508

    Google Scholar 

  • Holling CS (1959) The components of predation as revealed by a study of small-mammal predation of the European sawfly. Can Entomol 91:293–320

    Article  Google Scholar 

  • Johnson DW (2006) Predation, habitat complexity, and variation in density-dependent mortality of temperate reef fishes. Ecology 87:1179–1188

    Article  PubMed  Google Scholar 

  • Jonsson N, Jonsson B, Hansen LP (1998) The relative role of density-dependent and density-independent survival in the life cycle of Atlantic salmon Salmo salar. J Anim Ecol 67:751–762

    Article  Google Scholar 

  • Karels TJ, Byrom AE, Boonstra R, Krebs CJ (2000) The interactive effects of food and predators on reproduction and overwinter survival of arctic ground squirrels. J Anim Ecol 69:235–247

    Article  Google Scholar 

  • Kennedy BP, Klaue B, Blum JD, Folt C (2004) Integrative measures of consumption rates in salmon: expansion and application of a trace element approach. J Appl Ecol 41:1009–1020

    Article  Google Scholar 

  • Kocik JF, Ferreri CP (1998) Juvenile production variation in salmonids: population dynamics, habitat, and the role of spatial relationships. Can J Fish Aquat Sci 55:191–200

    Article  Google Scholar 

  • Le Cren ED (1973) The population dynamics of young trout (Salmo trutta) in relation to density and territorial behavior. Rapports et Proces-Verbaux des Reunions, Conseil International pour L’exploration de la Mer 164:241–246

    Google Scholar 

  • Letcher BH, Dubreuil T, O’Donnell MJ, Obedzinski M, Griswold K, Nislow KH (2004) Long-term consequences of variation in timing and manner of fry introduction on juvenile Atlantic salmon (Salmo salar) growth, survival, and life-history expression. Can J Fish Aquat Sci 61:2288–2301

    Article  Google Scholar 

  • Lobon-Cervia J, Rincon PA (2004) Environmental determinants of recruitment and their influence on the population dynamics of stream-living brown trout Salmo trutta. Oikos 105:641–646

    Article  Google Scholar 

  • Mather ME, Parrish DL, Folt CL, DeGraaf RM (1998) Integrating across scales: effectively applying science for the successful conservation of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 55:1–8

    Article  Google Scholar 

  • McMenemy JR (1995) Survival of Atlantic salmon fry stocked at low density in the West River, Vermont. North Am J Fish Manage 15:366–374

    Article  Google Scholar 

  • Milner NJ, Elliott JM, Armstrong JD, Gardiner R, Welton JS, Ladle M (2003) The natural control of salmon and trout populations in streams. Fish Res 62:111–125

    Article  Google Scholar 

  • Mirza RS, Chivers DP (2000) Predator-recognition training enhances survival of brook trout: evidence from laboratory and field-enclosure studies. Can J Zool 78:2198–2208

    Article  Google Scholar 

  • Mirza RS, Chivers DP, Godin JGJ (2001) Brook charr alevins alter timing of nest emergence in response to chemical cues from fish predators. J Chem Ecol 27:1775–1785

    Article  PubMed  CAS  Google Scholar 

  • Morgan CR, Ringler NH (1992) Experimental manipulation of sculpin (Cottus cognatus) populations in a small stream. J Freshw Ecol 7:227–232

    Google Scholar 

  • Moyle PB (1977) In defense of sculpins. Fisheries 2:20–23

    Article  Google Scholar 

  • Murdoch WW, Oaten A (1975) Predation and population stablility. Adv Ecol Res 9:1–132

    Google Scholar 

  • Naiman RJ, Bilby RE, Schindler DE, Helfield JM (2002) Pacific salmon, nutrients, and the dynamics of freshwater and riparian ecosystems. Ecosystems 5:399–417

    Article  Google Scholar 

  • Nehlsen W, Williams JE, Lichatowich JA (1991) Pacific salmon at the crossroads: stocks at risk from California, Oregon, Idaho, and Washington. Fisheries 16:4–21

    Google Scholar 

  • Nislow KH, Folt C, Seandel M (1998) Food and foraging behavior in relation to microhabitat use and survival of age-0 Atlantic salmon. Can J Fish Aquat Sci 55:116–127

    Article  Google Scholar 

  • Nislow KH, Folt CL, Parrish DL (2000) Spatially explicit bioenergetic analysis of habitat quality for age-0 Atlantic salmon. Trans Am Fish Soc 129:1067–1081

    Article  Google Scholar 

  • Nislow KH, Einum S, Folt C (2004) Testing predictions of the critical period for survival concept using experiments with stocked Atlantic salmon. J Fish Biol 65[Suppl A]:1–13

    Google Scholar 

  • Osenberg CW, St Mary CM, Schmitt RJ, Holbrook SJ, Chesson P, Byrne B (2002) Rethinking ecological inference: density dependence in reef fishes. Ecol Lett 5:715–721

    Article  Google Scholar 

  • Sandin SA, Pacala SW (2005) Fish aggregation results in inversely density-dependent predation on continuous coral reefs. Ecology 86:1520–1530

    Article  Google Scholar 

  • Schmitt RJ, Holbrook SJ (2007) The scale and cause of spatial heterogeneity in strength of temporal density dependence. Ecology 88:1241–1249

    Article  PubMed  Google Scholar 

  • Shepherd JG, Cushing DH (1990) Regulation in fish populations: myth or mirage. Philos Trans R Soc B 330:151–164

    Article  Google Scholar 

  • Shima JS, Osenberg CW (2003) Cryptic density dependence: effects of covariation between density and site quality in reef fish. Ecology 84:46–52

    Article  Google Scholar 

  • Sinclair ARE, Pech RP (1996) Density dependence, stochasticity, compensation and predator regulation. Oikos 75:164–173

    Article  Google Scholar 

  • Sinclair ARE, Pech RP, Dickman CR, Hik D, Mahon P, Newsome AE (1998) Predicting effects of predation on conservation of endangered prey. Conserv Biol 12:564–575

    Article  Google Scholar 

  • Symons PEK (1979) Estimated escapement of Atlantic salmon (Salmo salar) for maximum smolt production in rivers of different productivity. J Fish Res Board Can 36:132–140

    Google Scholar 

  • Utzinger J, Roth C, Peter A (1998) Effects of environmental parameters on the distribution of bullhead Cottus gobio with particular consideration of the effects of obstructions. J Appl Ecol 35:882–892

    Article  Google Scholar 

  • Varley GC, Gradwell GR (1960) Key factors in population studies. J Anim Ecol 29:399–401

    Article  Google Scholar 

  • Walters CJ, Juanes F (1993) 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 50:2058–2070

    Article  Google Scholar 

  • Ward DM (2007) Linking density-dependent survival and growth of juvenile Atlantic salmon to their predators and prey. PhD thesis. Dartmouth College, Hanover

  • Ward DM, Nislow KH, Folt C (2008) Do native species limit survival of reintroduced Atlantic salmon in historic rearing streams? Biol Conserv 141:146–152

    Article  Google Scholar 

  • Whalen KG, Parrish DL, Mather ME, McMenemy JR (2000) Cross-tributary analysis of parr to smolt recruitment of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 57:1607–1616

    Article  Google Scholar 

  • Zanette L, Smith JNM, van Oort H, Clinchy M (2003) Synergistic effects of food and predators on annual reproductive success in song sparrows. Proc R Soc B 270:799–803

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors thank the many people who assisted with field work, particularly Jim Sotiropolous, Gonzalo Mendez, Jon Raffensperger, and Karl Dietrich. Numerous landowners graciously allowed access to study sites. John Armstrong, Matt Ayres, Doug Bolger, and anonyomous reviewers provided helpful comments on an earlier draft. This work was supported by the USDA–USFS Northeastern Research Station, NIEHS-SBRP grant ES07373, an Atlantic Salmon Federation Olin fellowship, and the Dartmouth College Cramer fund. This research was conducted with approval from the Institutional Animal Care and Use Committee at Dartmouth College and conforms to the legal requirements of the United States.

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Correspondence to Darren M. Ward.

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Communicated by Craig Osenberg.

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Ward, D.M., Nislow, K.H. & Folt, C.L. Predators reverse the direction of density dependence for juvenile salmon mortality. Oecologia 156, 515–522 (2008). https://doi.org/10.1007/s00442-008-1011-4

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  • DOI: https://doi.org/10.1007/s00442-008-1011-4

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