Skip to main content
SpringerLink
Log in

Patterns of selective predation change with ontogeny but not density in a marine fish

  • Population ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Phenotypic variation is prevalent in the early life-history stages of many organisms and provides the basis for selective mortality on size and growth-related traits of older life stages. Densities of organisms can vary widely at important life-history transitions, raising additional questions about the interplay between selection and density-dependent processes. We evaluate density dependence in patterns of selective mortality for a temperate reef fish. Specifically, we exposed pre-settlement and post-settlement stages of the common triplefin (Forsterygion lapillum) to a natural predator and evaluated patterns of selective mortality on early life-history traits as a function of ontogenetic stage and density. We used otoliths to reconstruct the traits of fish that survived versus fish that were consumed (i.e., we recovered otoliths from the guts of predators), and we estimated selection by analysing the relationship between absolute fitness and standardised traits. Absolute fitness was negatively correlated with size and larval growth rate for pre-settlement fish (i.e., larger and faster growing individuals were more likely to be consumed by predators), and this was consistent across the range of densities evaluated. Post-settlement fish experienced no selective mortality. Additionally, absolute fitness was equal across density treatments, suggesting mortality was density-independent. Collectively, these results suggest that patterns of selection change with ontogeny, but may be stable across densities when mortality is density-independent. Shifts in selective mortality for species with distinct life-stages can mask and complicate relationships between traits and fitness, and the importance of such traits may be underappreciated for earlier life stages.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Almany GR, Webster MS (2006) The predation gauntlet: early post-settlement mortality in reef fishes. Coral Reefs 25:19–22

    Article  Google Scholar 

  • Anderson JT (1988) A review of size dependent survival during pre-recruit stages of fishes in relation to recruitment. J Northwest Atl Fish Sci 8:55–66

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Biro PA, Abrahams MV, Post JR, Parkinson EA (2004) Predators select against high growth rates and risk-taking behaviour in domestic trout populations. Proc R Soc B Biol Sci 271:2233–2237

    Article  Google Scholar 

  • Biro PA, Abrahams MV, Post JR, Parkinson EA (2006) Behavioural trade-offs between growth and mortality explain evolution of submaximal growth rates. J Anim Ecol 75:1165–1171

    Article  Google Scholar 

  • Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75:385–407

    Article  CAS  Google Scholar 

  • Brodie ED, Moore A, Janzen F (1995) Visualizing and quantifying natural selection. Trends Ecol Evol 10:313–318

    Article  Google Scholar 

  • Caie PKJ (2016) Selective mortality on early life-history traits of a temperate reef fish. MSc thesis, School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealand

  • Carlson SM, Quinn TP (2007) Ten years of varying lake level and selection on size-at-maturity in sockeye salmon. Ecology 88:2620–2629

    Article  Google Scholar 

  • Creel S, Winnie JA Jr (2005) Responses of elk herd size to fine-scale spatial and temporal variation in the risk of predation by wolves. Anim Behav 69:1181–1189

    Article  Google Scholar 

  • Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116

    Article  Google Scholar 

  • Downes SJ (2002) Size-dependent predation by snakes: selective foraging or differential prey vulnerability? Behav Ecol 13:551–560

    Article  Google Scholar 

  • Elzhov TV, Mullen KM, Spiess A-N, Bolker BM (2013) R interface to the Levenberg–Marquardt nonlinear least-squares algorithm found in MINPACK, plus support for bounds

  • Festa-Bianchet M, Jorgenson JT, Réale D (2000) Early development, adult mass, and reproductive success in bighorn sheep. Behav Ecol 11:633–639

    Article  Google Scholar 

  • Forrester GE, Steele MA (2004) Predators, prey refuges, and the spatial scaling of density-dependent prey mortality. Ecology 85:1332–1342

    Article  Google Scholar 

  • Forsgren E, Kvarnemo C, Lindstrom K (1996) Mode of sexual selection determined by resource abundance in two sand goby populations. Evolution 50:646–654

    Article  Google Scholar 

  • Gagliano M, McCormick MI, Meekan MG (2007) Survival against the odds: ontogenetic changes in selective pressure mediate growth-mortality trade-offs in a marine fish. Proc R Soc B Biol Sci 274:1575–1582

    Article  Google Scholar 

  • Gleason TR, Bengtson DA (1996) Size-selective mortality of inland silversides: evidence from otolith microstructure. Trans Am Fish Soc 125:860–873

    Article  Google Scholar 

  • Grorud-Colvert K, Sponaugle S (2011) Variability in water temperature affects trait-mediated survival of a newly settled coral reef fish. Oecologia 165:675–686

    Article  Google Scholar 

  • Hansen AG, Beauchamp DA (2014) Effects of prey abundance, distribution, visual contrast and morphology on selection by a pelagic piscivore. Freshw Biol 59:2328–2341

    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, Anderson TW, Buch KL, Johnson DW, McLeod JB, Stallings CD (2012) Density dependence and population regulation in marine fish: a large-scale, long-term field manipulation. Ecol Monogr 82:467–489

    Article  Google Scholar 

  • Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, Hoang A, Hill CE, Beerli P, Kingsolver JG (2001) Strength and tempo of directional selection in the wild. Proc Natl Acad Sci 98:9157–9160

    Article  CAS  Google Scholar 

  • Holbrook SJ, Schmitt RJ (2002) Competition for shelter space causes density-dependent predation mortality in damselfishes. Ecology 83:2855–2868

    Article  Google Scholar 

  • Holmes TH, McCormick MI (2006) Location influences size-selective predation on newly settled reef fish. Mar Ecol Prog Ser 317:203–209

    Article  Google Scholar 

  • Holmes TH, McCormick MI (2010) Size-selectivity of predatory reef fish on juvenile prey. Mar Ecol Prog Ser 399:273–283

    Article  Google Scholar 

  • Houde E (1987) Fish early life dynamics and recruitment variability. Am Fish Soc Symp 2:17–29

    Google Scholar 

  • Janzen FJ, Stern HS (1998) Logistic regression for empirical studies of multivariate selection. Evolution 52:1564–1571

    Article  Google Scholar 

  • Johnson DW, Hixon MA (2010) Ontogenetic and spatial variation in size-selective mortality of a marine fish. J Evol Biol 23:724–737

    Article  CAS  Google Scholar 

  • Johnson DW, Grorud-Colvert K, Rankin TL, Sponaugle S (2012) Measuring selective mortality from otoliths and similar structures: a practical guide for describing multivariate selection from cross-sectional data. Mar Ecol Prog Ser 471:151–163

    Article  Google Scholar 

  • Johnson DW, Grorud-Colvert K, Sponaugle S, Semmens BX (2014) Phenotypic variation and selective mortality as major drivers of recruitment variability in fishes. Ecol Lett 17:743–755

    Article  Google Scholar 

  • Kingsolver JG, Pfennig DW (2007) Patterns and power of phenotypic selection in nature. Bioscience 57:561–572

    Article  Google Scholar 

  • Kingsolver JG, Diamond SE, Siepielski AM, Carlson SM (2012) Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions. Evol Ecol 26:1101–1118

    Article  Google Scholar 

  • Krist M (2010) Egg size and offspring quality: a meta-analysis in birds. Biol Rev 86:692–716

    Article  Google Scholar 

  • Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226

    Article  Google Scholar 

  • Lázaro A, Traveset A (2009) Does the spatial variation in selective pressures explain among-site differences in seed mass? A test with Buxus balearica. Evol Ecol 23:847–865

    Article  Google Scholar 

  • Lorenzen K, Enberg K (2002) Density-dependent growth as a key mechanism in the regulation of fish populations: evidence from among-population comparisons. Proc R Soc B Biol Sci 269:49–54

    Article  Google Scholar 

  • Lundvall D, Svanbäck R, Persson L, Byström P (1999) Size-dependent predation in piscivores: interactions between predator foraging and prey avoidance abilities. Can J Fish Aquat Sci 56:1285–1292

    Article  Google Scholar 

  • Marshall DJ, Keough MJ (2007) The evolutionary ecology of offspring size in marine invertebrates. Adv Mar Biol 53:1–60

    Article  Google Scholar 

  • Marshall DJ, Morgan SG (2011) Ecological and evolutionary consequences of linked life-history stages in the sea. Curr Biol 21:R718–R725

    Article  CAS  Google Scholar 

  • Marshall DJ, Pechenik JA, Keough MJ (2003) Larval activity levels and delayed metamorphosis affect post-larval performance in the colonial ascidian Diplosoma listerianum. Mar Ecol Prog Ser 246:153–162

    Article  Google Scholar 

  • McCormick MI, Meekan MG (2007) Social facilitation of selective mortality. Ecology 88:1562–1570

    Article  Google Scholar 

  • McDermott CJ, Shima JS (2006) Ontogenetic shifts in microhabitat preference of the temperate reef fish Forsterygion lapillum—implications for population limitation. Mar Ecol Prog Ser 320:259–266

    Article  Google Scholar 

  • Meekan MG, Fortier L (1996) Selection for fast growth during the larval life of Atlantic cod Gadus morhua on the Scotian Shelf. Mar Ecol Prog Ser 137:25–37

    Article  Google Scholar 

  • Meekan MG, von Kuerthy C, McCormick MI, Radford B (2010) Behavioural mediation of the costs and benefits of fast growth in a marine fish. Anim Behav 79:803–809

    Article  Google Scholar 

  • Mensink PJ, Shima JS (2014) Patterns of co-occurance and interactions between age classes of the common triplefin, Fostergyion lapillum. Mar Biol 161:1285–1298

    Article  Google Scholar 

  • Miller TJ, Crowder LB, Rice JA, Marschall EA (1988) Larval size and recruitment mechanisms in fishes: toward a conceptual framework. Can J Fish Aquat Sci 45:1657–1670

    Article  Google Scholar 

  • Moginie BF, Shima JS (2018) Hatch date and growth rate drives reproductive success in nest-guarding males of a temperate reef fish. Mar Ecol Prog Ser 592:197–206

    Article  Google Scholar 

  • Morton DC, Shima JS (2013) Habitat configuration and availability influences the settlement of temperate reef fishes (Tripterygiidae). J Exp Mar Biol Ecol 449:215–220

    Article  Google Scholar 

  • Murphy HM, Warren-Myers FW, Jenkins GP, Hamer PA, Swearer SE (2014) Variability in size-selective mortality obscures the importance of larval traits to recruitment success in a temperate marine fish. Oecologia 175:1201–1210

    Article  Google Scholar 

  • Noonburg EG, Chen A, Shima JS, Swearer SE (2015) Demographic heterogeneity and the dynamics of open populations. Ecology 96:1159–1165

    Article  Google Scholar 

  • Pechenik JA (2006) Larval experience and latent effects—metamorphosis is not a new beginning. Integr Comp Biol 46:323–333

    Article  Google Scholar 

  • Pepin P (1989) Predation and starvation of larval fish: a numerical experiment of size- and growth-dependent survival. Biol Oceanogr 6:23–44

    Google Scholar 

  • Pepin P, Shears TH, de Lafontaine Y (1992) Significance of body size to the interaction between a larval fish (Mallotus villosus) and a vertebrate predator (Gasterosteus aculeatus). Mar Ecol Prog Ser 81:1–12

    Article  Google Scholar 

  • Perez KO, Munch SB (2010) Extreme selection on size in the early lives of fish. Evolution 64:2450–2457

    PubMed  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rankin TL, Sponaugle S (2011) Temperature influences selective mortality during the early life stages of a coral reef fish. PLoS One 6:e16814

    Article  CAS  Google Scholar 

  • Rey PJ, Garrido JL, Alcántara JM, Ramírez JM, Aguilera A, García L, Manzaneda AJ, Fernández R (2002) Spatial variation in ant and rodent post-dispersal predation of vertebrate-dispersed seeds. Funct Ecol 16:773–781

    Article  Google Scholar 

  • Rice JA, Miller TJ, Crowder LB, Marschall EA, Trebitz AS, DeAngelis DL (1993) Growth rate variation and larval survival: inferences from an individual-based size-dependent predation model. Can J Fish Aquat Sci 50:133–142

    Article  Google Scholar 

  • Robert D, Castonguay M, Fortier L (2007) Early growth and recruitment in Atlantic mackerel Scomber scombrus: discriminating the effects of fast growth and selection for fast growth. Mar Ecol Prog Ser 337:209–219

    Article  Google Scholar 

  • RStudio Team (2015) RStudio: integrated development environment for R. RStudio Inc., Boston

    Google Scholar 

  • Samhouri JF, Steele MA, Forrester GE (2009) Inter-cohort competition drives density dependence and selective mortality in a marine fish. Ecology 90:1009–1020

    Article  Google Scholar 

  • Searcy SP, Sponaugle S (2001) Selective mortality during the larval–juvenile transition in two coral reef fishes. Ecology 82:2452–2470

    Google Scholar 

  • Shima JS, Findlay AM (2002) Pelagic larval growth rate impacts benthic settlement and survival of a temperate reef fish. Mar Ecol Prog Ser 235:303–309

    Article  Google Scholar 

  • Shima JS, Swearer SE (2009) Larval quality is shaped by matrix effects—implications for connectivity in a marine metapopulation. Ecology 90:1255–1267

    Article  Google Scholar 

  • Shima JS, Swearer SE (2010) The legacy of dispersal: larval experience shapes persistence later in the life of a reef fish. J Anim Ecol 79:1308–1314

    Article  Google Scholar 

  • Shima JS, Swearer SE (2016) Evidence and population consequences of shared larval dispersal histories in a marine fish. Ecology 97:25–31

    Article  Google Scholar 

  • Shima JS, Noonburg EG, Phillips NE (2010) Life history and matrix heterogeneity interact to shape metapopulation connectivity in spatially structured environments. Ecology 91:1215–1224

    Article  Google Scholar 

  • Shima JS, Noonburg EG, Swearer SE (2015) Consequences of variable larval dispersal pathways and resulting phenotypic mixtures to the dynamics of marine metapopulations. Biol Lett 11:20140778

    Article  Google Scholar 

  • Shulzitski K, Sponaugle S, Hauff M, Walter KD, Cowen RK (2016) Encounter with mesoscale eddies enhances survival to settlement in larval coral reef fishes. Proc Natl Acad Sci 113:6928–6933

    Article  CAS  Google Scholar 

  • Siepielski AM, DiBattista JD, Carlson SM (2009) It’s about time: the temporal dynamics of phenotypic selection in the wild. Ecol Lett 12:1261–1276

    Article  Google Scholar 

  • Smith AC, Shima JS (2011) Variation in the effects of larval history on juvenile performance of a temperate reef fish. Austral Ecol 36:830–838

    Article  Google Scholar 

  • Sogard SM (1997) Size-selective mortality in the juvenile stage of teleost fishes: a review. Bull Mar Sci 60:1129–1157

    Google Scholar 

  • Sponaugle S, Boulay JN, Rankin TL (2011) Growth- and size-selective mortality in pelagic larvae of a common reef fish. Aquat Biol 13:263–273

    Article  Google Scholar 

  • Staudinger MD, Juanes F (2010) Size-dependent susceptibility of longfin inshore squid (Loligo pealeii) to attack and capture by two predators. J Exp Mar Biol Ecol 393:106–113

    Article  Google Scholar 

  • Sun Z, Hamel J-F, Parrish CC, Mercier A (2015) Complex offspring size effects: variations across life stages and between species. Ecol Evol 5:1117–1129

    Article  Google Scholar 

  • Swearer S, Shima JS (2010) Regional variation in larval retention and dispersal drives recruitment patterns in a temperate reef fish. Mar Ecol Prog Ser 417:229–236

    Article  Google Scholar 

  • Takasuka A, Ichiro A, Mitani I (2007) Evidence of growth-selective predation on larval Japanese anchovy Engraulis japonicus in Sagami Bay. Mar Ecol Prog Ser 252:223–238

    Article  Google Scholar 

  • Thompson JN (1999) Specific hypotheses on the geographic mosaic of coevolution. Am Nat 153:S1–S14

    Article  Google Scholar 

  • Vigliola L, Meekan MG (2002) Size at hatching and planktonic growth determine post-settlement survivorship of a coral reef fish. Oecologia 131:89–93

    Article  Google Scholar 

  • Wellenreuther M, Clements KD (2008) Determinants of habitat association in a sympatric clade of marine fishes. Mar Biol 154:393–402

    Article  Google Scholar 

Download references

Acknowledgements

We thank three anonymous reviewers for their helpful comments on an earlier draft of this manuscript. Funding was provided by a Marsden Grant awarded to J. Shima. This work was carried out in accordance with the Victoria University of Wellington (Permit no. 22038) Animal Ethics Committee. Research assistance was provided by the Shima lab at Victoria University of Wellington, special thanks to B. Moginie and B. Focht for assistance in the field. Logistical assistance was provided by the Victoria University Coastal Ecology Laboratory. The dataset analysed in this study available from the corresponding author on reasonable request.

Author information

Authors and Affiliations

  1. School of Biological Sciences, Victoria University of Wellington, PO Box 600, Wellington, New Zealand

    Phoebe Caie & Jeffrey S. Shima

Authors
  1. Phoebe Caie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeffrey S. Shima
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

PC and JSS conceived and designed the experiments. PC conducted fieldwork, performed the experiments and analysed the data. PC and JSS wrote the manuscript.

Corresponding author

Correspondence to Phoebe Caie.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Nicole Phillips.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Caie, P., Shima, J.S. Patterns of selective predation change with ontogeny but not density in a marine fish. Oecologia 189, 123–132 (2019). https://doi.org/10.1007/s00442-018-4303-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-018-4303-3

Keywords

Search

Navigation