Skip to main content
SpringerLink
Log in

Does a bigger mouth make you fatter? Linking intraspecific gape variability to body condition of a tropical predatory fish

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

Abstract

In gape-limited predators, gape size restricts the maximum prey size a predator is capable to ingest. However, studies investigating the energetic consequences of this relationship remain scarce. In this study, we tested the hypothesis that gape-size variability influences individual body condition (a common proxy for fitness) in one of the largest freshwater teleost predators, the barramundi. We found that individual barramundi with larger gapes relative to body size had higher body condition values compared to conspecifics with smaller gapes. Body condition was highest soon after the wet season, a period of high feeding activity on productive inundated floodplains, and body condition decreased as the dry season progressed when fish were restricted to dry season remnant habitats. The increased condition obtained during the wet season apparently offsets weight loss through the dry season, as individuals with large gapes were still in better condition than fish with small gapes in the late-dry season. Elucidation of the links between intraspecific variability in traits and performance is a critical challenge in functional ecology. This study emphasizes that even small intraspecific variability in morphological trait values can potentially affect individual fitness within a species’ distribution.

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

Similar content being viewed by others

References

  • Albouy C, Guilhaumon F, Villéger S, Mouchet M, Mercier L, Culioli J, Tomasini J, Le Loc’h F, Mouillot D (2011) Predicting trophic guild and diet overlap from functional traits: statistics, opportunities and limitations for marine ecology. Mar Ecol Prog Ser 436:17–28

    Article  Google Scholar 

  • Anderson JT, Saldaña-Rojas J, Flecker AS (2009) High-quality seed dispersal by fruit-eating fishes in Amazonian floodplain habitats. Oecologia 161:279–290

    Article  PubMed  Google Scholar 

  • Arrington DA, Winemiller KO, Layman CA (2005) Community assembly at the patch scale in a species rich tropical river. Oecologia 144:157–167

    Article  PubMed  Google Scholar 

  • Balcombe SR, Lobegeiger JS, Marshall SM, Marshall JC, Ly D, Jones DN (2012) Fish body condition and recruitment success reflect antecedent flows in an Australian dryland river. Fish Sci 78:841–847

    Article  CAS  Google Scholar 

  • Balcombe SR, Arthington AH, Sternberg D (2014) Fish body condition and recruitment responses to antecedent flows in dryland rivers are species and river specific. River Res Appl 30:1257–1268

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H, Dai B, Scheipl F, Grothendieck G, Green P, Fox J (2018) Linear mixed-effects models using ‘Eigen’ and S4. R Package ‘lme4’.https://cran.r-project.org/web/packages/lme4/. Accessed 26 Nov 2018

  • Bishop KA, Allen SA, Pollard DA, Cook MG (2001) Ecological studies on the freshwater fishes of the Alligator rivers region, northern territory: autecology. supervising scientist report 145, Supervising scientist, Darwin

  • Blanck A, Lamouroux N (2007) Large scale intraspecific variation in life history traits of European freshwater fish. J Biogeogr 34:862–875

    Article  Google Scholar 

  • Bolger T, Connolly PL (1989) The selection of suitable indices for the measurement and analysis of fish condition. J Fish Biol 34:171–182

    Article  Google Scholar 

  • Cattau CE, Fletcher RJ Jr, Kimball RT, Miller CW, Kitchens WM (2018) Rapid morphological change of a top predator with the invasion of a novel prey. Nat Ecol Evol 2:108–115

    Article  PubMed  Google Scholar 

  • Cooper WJ, Carter CB, Conith AJ, Rice AN, Westneat MW (2017) The evolution of jaw protrusion mechanics is tightly coupled to bentho-pelagic divergence in damselfishes (Pomacentridae). J Exp Biol 220:652–666

    Article  PubMed  Google Scholar 

  • Crook DA, Buckle DJ, Allsop Q, Baldwin W, Saunders TM, Kyne PM, Woodhead JD, Maas R, Roberts B, Douglas MM (2017) Use of otolith chemistry and acoustic telemetry to elucidate migratory contingents in barramundi Lates calcarifer. Mar Freshw Res 68:1554–1566

    Article  Google Scholar 

  • Davis TLO (1985) The food of barramundi, Lates calcarifer (Bloch), in coastal and inland waters of Van Diemen Gulf and the Gulf of Carpentaria, Australia. J Fish Biol 26:669–682

    Article  Google Scholar 

  • Des Roches S, Post DM, Turley NE, Bailey JK, Hendry AP, Kinnison MT, Schweitzer JA, Palkovacs EP (2018) The ecological importance of intraspecific variation. Nat Ecol Evol 2:57–64

    Article  PubMed  Google Scholar 

  • Detmer TM, Einfalt LM, Parkos JJ, Wahl DH (2018) Comparison of mouth morphology and prey size selection among three esocid taxa. Environ Biol Fish 101:1–10

    Article  Google Scholar 

  • Ebner BC, Morgan DL, Kerezsy A, Hardie S, Beatty SJ, Seymour JE, Donaldson JA, Linke S, Peverell S, Roberts D, Espinoza T (2016) Enhancing conservation of Australian freshwater ecosystems: identification of freshwater flagship fishes and relevant target audiences. Fish Fish 17:1134–1151

    Article  Google Scholar 

  • Ehlinger TJ, Wilson D (1988) Complex foraging polymorhphism in bluegill sunfish. Proc Natl Acad Sci 85:1878–1882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forsman A (1996) Body size and net energy gain in gape-limited predators: a model. J Herpetol 30:307–319

    Article  Google Scholar 

  • Forsman A, Shine R (1997) Rejection of non-adaptive hypotheses for intraspecific variation in trophic morphology in gape-limited predators. Biol J Linn Soc 62:209–223

    Article  Google Scholar 

  • Gatz AJ (1979) Ecological morphology of freshwater stream fishes. Tulane Stud Zool Bot 21:91–124

    Google Scholar 

  • Gerking SD (1994) Feeding ecology of fish. Academic Press, California

    Google Scholar 

  • Hall ES, Martin BE, Brubaker K, Grant CJ (2018) Latitudinal variation in the geometric morphology of the largemouth bass, Micropterus salmoides. Mar Freshw Res 69:1480–1485

    Article  Google Scholar 

  • Hambright KD (1991) Experimental analysis of prey selection by largemouth bass: role of predator mouth width and prey body depth. Trans Am Fish Soc 120:500–508

    Article  Google Scholar 

  • Hobson ES (1979) Interactions between piscivorous fishes and their prey. In: Clepper H, Stroud RH (eds) Predator–Prey systems in fisheries management. Sport Fishing Institute, DC, pp 231–242

    Google Scholar 

  • Hoeinghaus DJ, Winemiller KO, Layman CA, Arrington DA, Jepsen DB (2006) Effects of seasonality and migratory prey on body condition of Cichla species in a tropical floodplain river. Ecol Freshw Fish 15:398–407

    Article  Google Scholar 

  • Jakob EM, Marshall SD, Uetz GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61–67

    Article  Google Scholar 

  • Jardine TD, Pettit NE, Warfe DM, Pusey BJ, Ward DP, Douglas MM, Davies PM, Bunn SE (2012) Consumer–resource coupling in wet–dry tropical rivers. J Anim Ecol 81:310–322

    Article  PubMed  Google Scholar 

  • Juanes F (1994) What determines prey size selectivity in piscivorous fishes? In: Stouder DJ, Fresh KL, Feller R (eds) Theory and application in fish feeding ecology. University of South Carolina Press, South Carolina, pp 77–100

    Google Scholar 

  • Juanes F, Buckel JA, Scharf FS (2002) Feeding ecology of piscivorous fishes. In: Hart P, Reynolds JD (eds) Handbook of fish biology and fisheries: fish biology, 1st edn. Blackwell Scientific, Oxford, pp 267–283

    Chapter  Google Scholar 

  • Karpouzi VS, Stergiou KI (2003) The relationships between mouth size and shape and body length for 18 species of marine fishes and their trophic implications. J Fish Biol 62:1353–1365

    Article  Google Scholar 

  • Kennard MJ, Pusey BJ, Olden JD, Mackay SJ, Stein JL, Marsh N (2010) Classification of natural flow regimes in Australia to support environmental flow management. Freshw Biol 55:171–193

    Article  Google Scholar 

  • Kristjánsson B, Skúlason S, Noakes DLG (2002) Rapid divergence in a recently isolated population of threespine stickleback (Gasterosteus aculeatus L.). Evol Ecol Res 4:659–672

    Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2018) Tests in linear mixed effects models. R package ‘lmerTest’. https://cran.r-project.org/web/packages/lmerTest/. Accessed 26 Nov 2018

  • Magnhagen C, Heino E (2001) Gape size allometry in pike reflects variation between lakes in prey availability and relative body depth. Funct Ecol 15:754–762

    Article  Google Scholar 

  • Maret TJ, Collins JP (1996) Effect of prey vulnerability on population size structure of a gape-limited predator. Ecology 77:320–324

    Article  Google Scholar 

  • McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185

    Article  PubMed  Google Scholar 

  • Messier J, McGill BJ, Lechowicz MJ (2010) How do traits vary across ecological scales? A case for trait-based ecology. Ecol Lett 13:838–848

    Article  PubMed  Google Scholar 

  • Miehls AL, Peacor SD, McAdam AG (2014) Gape-limited predators as agents of selection on the defensive morphology of an invasive invertebrate. Evolution 68:2633–2643

    Article  PubMed  Google Scholar 

  • Mihalitsis M, Bellwood DR (2017) A morphological and functional basis for maximum prey size in piscivorous fishes. PLoS One 12:e0184679

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nilsson PA, Brönmark C (2000) Prey vulnerability to a gape-size limited predator: behavioural and morphological impacts on northern pike piscivory. Oikos 88:39–546

    Google Scholar 

  • Norin T, Clark TD (2017) Fish face a trade-off between ‘eating big’ for growth efficiency and ‘eating small’ to retain aerobic capacity. Biol Lett 13:20170298

    Article  PubMed  PubMed Central  Google Scholar 

  • Norton SF (1995) A functional approach to ecomorphological patterns of feeding in cottid fishes. Environ Biol Fish 44:61–78

    Article  Google Scholar 

  • Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891

    Article  Google Scholar 

  • Persson L, Andersson J, Wahlstrom E, Eklov P (1996) Size-specific interactions in lake systems: predator gape limitation and prey growth rate and mortality. Ecology 77:900–911

    Article  Google Scholar 

  • Pettit NE, Naiman RJ, Warfe DM, Jardine TD, Douglas MM, Bunn SE, Davies PM (2017) Productivity and connectivity in tropical riverscapes of northern Australia: ecological insights for management. Ecosystems 20:492–514

    Article  Google Scholar 

  • Phillips B, Shine R (2004) Adapting to an invasive species: toxic cane toads induce morphological change in Australian snakes. Proc Natl Acad Sci 101:17150–17155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pope KL, Kruse CG (2007) Condition. In: Guy CS, Brown ML (eds) Analysis and interpretation of freshwater fisheries data. American Fisheries Society, Maryland, pp 423–471

    Google Scholar 

  • Pusey B, Kennard M, Arthington A (2004) Freshwater fishes of north–eastern Australia. CSIRO publishing, Australia

    Book  Google Scholar 

  • R Development Core Team (2019) R: a language and environment for statistical computing. See http://www.r-project.org. Accessed 26 Nov 2018

  • Saunders T, Whybird O, Newman S (2018) Status of key northern territory fish stocks report 2016. Northern territory government. Department of primary industry and resources. http://www.fish.gov.au/report/7-Barramundi-2016. Accessed 30 Nov 2018

  • Scharf FS, Juanes F, Rountree RA (2000) Predator size–prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic niche breadth. Mar Ecol Prog Ser 208:229–248

    Article  Google Scholar 

  • Schmitt RJ, Holbrook SJ (1984) Gape-limitation, foraging tactics and prey size selectivity of two microcarnivorous species of fish. Oecologia 63:6–12

    Article  PubMed  Google Scholar 

  • Sutton SG, Bult TP, Haedrich RL (2000) Relationships among fat weight, body weight, water weight, and condition factors in wild Atlantic salmon parr. Trans Am Fish Soc 129:527–538

    Article  Google Scholar 

  • Urban MC (2007) The growth–predation risk trade-off under a growing gape-limited predation threat. Ecology 88:2587–2597

    Article  PubMed  Google Scholar 

  • Vatland S, Budy P (2007) Predicting the invasion success of an introduced omnivore in a large, heterogeneous reservoir. Can J Fish Aquat Sci 64:1329–1345

    Article  Google Scholar 

  • Villéger S, Brosse S, Mouchet M, Mouillot D, Vanni MJ (2017) Functional ecology of fish: current approaches and future challenges. Aquat Sci 79:783–801

    Article  Google Scholar 

  • Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892

    Article  Google Scholar 

  • Violle C, Enquist BJ, McGill BJ, Jiang LIN, Albert CH, Hulshof C, Jung V, Messier J (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252

    Article  PubMed  Google Scholar 

  • Voshikawa T, Higuchi H (2018) Invasion of the loquat Eriobotrya japonica into urban areas of central Tokyo facilitated by crows. Ornithol Sci 17:165–172

    Article  Google Scholar 

  • Warfe DM, Pettit NE, Davies PM, Pusey BJ, Hamilton SK, Kennard MJ, Towsend SA, Bayliss P, Ward DP, Douglas MM, Burford MA, Finn M, Bunn SE, Halliday IA (2011) The ‘wet–dry’ in the wet–dry tropics drives river ecosystem structure and processes in northern Australia. Freshw Biol 56:2169–2195

    Article  Google Scholar 

  • Winemiller KO, Jepsen DB (1998) Effects of seasonality and fish movement on tropical river food webs. J Fish Biol 53:267–296

    Article  Google Scholar 

  • Xiao Y (2000) Use of the original von Bertalanffy growth model to describe the growth of barramundi, Lates calcarifer (Bloch). Fish Bull 98:835

    Google Scholar 

Download references

Acknowledgements

We thank B. Adair, K. Keller, D. Lowensteiner, Q. Allsop, W. Baldwin, C. Errity, N. Croft for assistance with field sampling, R. Morais and three anonymous reviews for comments that improved the manuscript, and B. Adair and D. Lowensteiner for assistance with fish measurement in the laboratory.

Funding

Financial support was provided by the Australian Research Council (LP150100388) and the Department of Primary Industry and Fisheries, Northern Territory Government.

Author information

Authors and Affiliations

  1. Research Institute for the Environment and Livelihoods, Charles Darwin University, Ellengowan Dr, Darwin, NT, 0810, Australia

    Osmar J. Luiz, David A. Crook, Thor M. Saunders, Michael M. Douglas, Dion Wedd & Alison J. King

  2. Australian Rivers Institute, Griffith University, Nathan, QLD, Australia

    Mark J. Kennard & Julian D. Olden

  3. School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA, USA

    Julian D. Olden

  4. Department of Primary Industry and Fisheries, Darwin, NT, Australia

    Thor M. Saunders

  5. School of Biological Sciences, School of Agriculture and Environment, The University of Western Australia, Perth, WA, Australia

    Michael M. Douglas

Authors
  1. Osmar J. Luiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David A. Crook
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark J. Kennard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Julian D. Olden
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thor M. Saunders
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michael M. Douglas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dion Wedd
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alison J. King
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AJK, DAC, JDO, MJK, MMD and TMS conceived the study. AJK, DW and OJL collected the data. OJL analyzed the data and wrote the first draft of the manuscript and all authors contributed to revisions.

Corresponding author

Correspondence to Osmar J. Luiz.

Additional information

Communicated by Joel Trexler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 573 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luiz, O.J., Crook, D.A., Kennard, M.J. et al. Does a bigger mouth make you fatter? Linking intraspecific gape variability to body condition of a tropical predatory fish. Oecologia 191, 579–585 (2019). https://doi.org/10.1007/s00442-019-04522-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-019-04522-w

Keywords

Search

Navigation