Skip to main content

Advertisement

SpringerLink
Log in

Trophic niches through ontogeny in 12 species of Indo-Pacific marine Clupeoidei (herrings, sardines, and anchovies)

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The trophic niche is an aspect of species biology that is foundational to understanding many biological processes. In coastal marine ecosystems, small schooling fishes have a large influence on food web dynamics and structure, but despite their importance, the trophic niches of many of these fishes are either completely unknown or only preliminarily described. We assembled a diet dataset for 12 species of small, coastal Indo-Pacific clupeoids (herrings, sardines, and anchovies) containing measurements of 12,401 prey items from 619 individual fish predators to address four objectives: (1) assign species to trophic guilds based upon prey-type and -size consumption, (2) identify ontogenetic shifts in prey-type and -size consumption, (3) test the hypotheses that niche breadth, measured as the range of prey sizes consumed, and relative niche breadth (ratio of niche breadth to predator size) are positively correlated with predator size, and (4) test the hypotheses that maximum prey-size consumption and relative maximum prey-size consumption (ratio of maximum prey size to predator size) are positively correlated with predator size. We identified three and five trophic guilds based upon prey types and prey sizes, respectively. Diets changed through ontogeny in nearly every species. Linear regression revealed positive correlations between niche breadth, maximum prey width, and relative maximum prey width and predator size, but did not find a statistically significant correlation between relative niche breadth and predator size. This study shows that measuring prey size in addition to prey type can offer additional, higher resolution information about fish trophic ecology. The dataset presented here will be useful for future ecological and evolutionary research and fisheries management.

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
Fig. 5

Similar content being viewed by others

References

  • Abrantes K, Sheaves M (2009) Food web structure in a near-pristine mangrove area of the Australian wet tropics. Estuar Coast Shelf Sci 82:597–607

    Article  CAS  Google Scholar 

  • Alcaraz M, Saiz E, Calbet A, Trepat I, Broglio E (2003) Estimating zooplankton biomass through image analysis. Mar Biol 143:307–315

    Article  Google Scholar 

  • Ayón P, Swartzman G, Espinoza P, Bertrand A (2011) Long-term changes in zooplankton size distribution in the Peruvian Humboldt Current System: conditions favouring sardine or anchovy. Mar Ecol Prog Ser 422:211–222

    Article  Google Scholar 

  • Baker R, Sheaves M (2005) Redefining the piscivore assemblage of shallow estuarine nursery habitats. Mar Ecol Prog Ser 291:197–213

    Article  Google Scholar 

  • Bray RJ, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349

    Article  Google Scholar 

  • Brosset P, Le Bourg B, Costalago D, Bănaru VanBeveren E, Bourdeix J-H, Fromentin J-M, Ménard F, Saraux C (2016) Linking small pelagic dietary shifts and ecosystem changes in the Gulf of Lions. Mar Ecol Prog Ser 554:157–171

    Article  Google Scholar 

  • Buchheister A, Latour RJ (2015) Diets and trophic-guild structure of a diverse fish assemblage in Chesapeake Bay, USA. J Fish Biol 86:967–992

    Article  CAS  Google Scholar 

  • Casini M, Hjelm J, Molinero J-C, Lövgren J, Cardinale M, Bartolino V, Belgrano A, Kornilovs G (2009) Trophic cascades promote threshold-like shifts in pelagic marine ecosystems. PNAS 106(1):197–202

    Article  CAS  Google Scholar 

  • Chacko PI (1949) Food and feeding habits of the fishes of the Gulf of Manaar. Proc Plant Sci 29(3):83–97

    Google Scholar 

  • Conway DVP, Coombs SH, Smith C (1998) Feeding of anchovy Engraulis encrasicolus larvae in the northwestern Adriatic Sea in response to changing hydrobiological conditions. Mar Ecol Prog Ser 175:35–49

    Article  Google Scholar 

  • Costalago D, Palomera I (2014) Feeding of European pilchard (Sardina pilchardus) in the northwestern Mediterranean: from late larvae to adults. Sci Mar 78(1):41–54

    Article  Google Scholar 

  • Costalago E, Garrido S, Palomera I (2015) Comparison of the feeding apparatus and diet of European sardines Sardinella pilchardus of Atlantic and Mediterranean waters: ecological implications. J Fish Biol 86:1348–1362

    Article  CAS  Google Scholar 

  • Crowder DW, Snyder WE (2010) Eating their way to the top? Mechanisms underlying the success of invasive insect generalist predators. Biol Invasions 12(9):2857–2876

    Article  Google Scholar 

  • Cury P, Bakun A, Crawford RJM, Jarre A, Quiñones RA, Shannon LJ, Verheye HM (2000) Small pelagics in upwelling systems: patterns of interaction and structural changes in “wasp-waist” ecosystems. ICES J Mar Sci 57:603–618

    Article  Google Scholar 

  • Daskalov GM, Grishin AN, Rodionov S, Mihneva V (2007) Trophic cascades triggered by overfishing reveal possible mechanisms of ecosystem regime shifts. PNAS 104(25):10518–10523

    Article  CAS  Google Scholar 

  • Day RD, German DP, Manjakasy JM, Farr I, Hansen MJ, Tibbetts IR (2011) Enzymatic digestion in stomachless fishes: how a simple gut accommodates both herbivory and carnivory. J Comp Physiol B 181:603–613

    Article  CAS  Google Scholar 

  • Devictor V, Clavel J, Julliard R, Lavergne S, Mouillot D, Thuiller W, Venail P, Villeger S, Mouquet N (2010) Defining and measuring ecological specialization. J Appl Ecol 47(1):15–25

    Article  Google Scholar 

  • Egan JP, Chew U-S, Kuo C-H, Villarroel-Diaz V, Hundt PJ, Iwinski NG, Hammer MP, Simons AM (2017) Diets and trophic guilds of small fishes from coastal marine habitats in western Taiwan. J Fish Biol 91(1):331–345

    Article  CAS  Google Scholar 

  • Egan JP, Bloom DD, Kuo C-H, Hammer MP, Tongnunui P, Iglésias SP, Sheaves M, Grudpan C, Simons AM (2018) Phylogenetic analysis of trophic niche evolution reveals a latitudinal herbivory gradient in Clupeoidei (herrings, anchovies, and allies). Mol Phylogenet Evol 124:151–161

    Article  Google Scholar 

  • Espinoza P, Bertrand A (2008) Revisiting Peruvian anchovy (Engraulis ringens) trophodynamics provides a new vision of the Humboldt Current system. Prog Oceanogr 79:215–227

    Article  Google Scholar 

  • Floeter SR, Behrens MD, Ferreira CEL, Paddack MJ, Horn MH (2005) Geographical gradients of marine herbivorous fishes: patterns and processes. Mar Biol 147:1435–1447

    Article  Google Scholar 

  • Gaines SD, Lubchenco J (1982) A unified approach to marine plant-herbivore interactions. II. Biogeography. Annu Rev Ecol Evol Syst 13:111–138

    Article  Google Scholar 

  • Gannon JE (1976) The effects of differential digestion rates of zooplankton by alewife, Alosa pseudoharengus, on determinations of selective feeding. Trans Am Fish Soc 105:89–95

    Article  Google Scholar 

  • Garrison LP, Link JS (2000) Dietary guild structure of the fish community in the north-east United States continental shelf ecosystem. Mar Ecol Prog Ser 202:231–240

    Article  Google Scholar 

  • Gravel D, Poisot T, Albouy C, Velez L, Mouillot D (2013) Inferring food web structure from predator-prey body size relationships. Methods Ecol Evol 4:1083–1090

    Article  Google Scholar 

  • Hajisamae S, Ibrahim S (2008) Seasonal and spatial variations of fish trophic guilds in a shallow, semi-enclosed tropical estuarine bay. Environ Biol Fish 82:251–264

    Article  Google Scholar 

  • Hayase S, Ichikawa T, Tanaka K (1999) Preliminary report on stable isotope ratio analysis for samples from Matang Mangrove brackish water ecosystems. Jpn Agric Res Q 33:215–221

    Google Scholar 

  • Henrique P, Pereira C, Barros B, Zemoi R, Ferreira BP (2014) Ontogenetic diet changes and food partitioning of Haemulon spp. coral reef fishes, with a review of the genus diet. Rev Fish Biol Fish. https://doi.org/10.1007/s11160-014-9378-2

    Article  Google Scholar 

  • Horinouchi M, Tongnunui P, Furumitsu K, Nakamura Y, Kanou K, Yamaguchi A, Okamoto K, Sano M (2012) Food habits of small fishes in seagrass habitats in Trang, southern Thailand. Fish Sci 78:577–587

    Article  CAS  Google Scholar 

  • Hothorn T, Zeileis A, Farebrother RW, Cummins C, Giovanni M, Mitchell D (2017) Package “lmtest”. https://cran.r-project.org/package=lmtest. Accessed 10 July 2018

  • Hubbs CL, Lagler KF (1941) Guide to the fishes of the great lakes tributary waters. Cranbrook Press, Bloomfield Hills

    Google Scholar 

  • Hundt PJ, Nakamura Y, Yamaoka K (2014) Diet of combtooth blennies (Blenniidae) in Kochi and Okinawa, Japan. Ichthyol Res 61:76–82

    Article  Google Scholar 

  • Hyslop EJ (1980) Stomach contents analysis—a review of methods and their application. J Fish Biol 17:411–429

    Article  Google Scholar 

  • Jaksić FM, Medel RG (1990) Objective recognition of guilds: testing for statistically significant species clusters. Oecologia 82:87–92

    Article  Google Scholar 

  • Jensen H, Kahilainen KK, Amundsen P-A, Gjelland KØ, Tuomaala A, Malinen T, Bøhn T (2008) Predation by brown trout (Salmo trutta) along a diversifying prey community gradient. Can J Fish Aqaut Sci 65:1831–1841

    Article  Google Scholar 

  • Koenker R, Ng PT, Zeileis A, Grosjean P, Ripley BD (2018) quantreg: Quantile Regression. R package version 5.36. https://CRAN.R-project.org/package=quantreg/. Accessed 20 July 2018

  • Krebs JM, Turingan RG (2003) Intraspecific variation in gape-prey size relationships and feeding success during early ontogeny in red drum, Sciaenops ocellatus. Environ Biol Fish 66:75–84

    Article  Google Scholar 

  • Lawlor LR (1980) Structure and stability in natural and randomly constructed competitive communities. Am Nat 116:394–408

    Article  Google Scholar 

  • Legendre P, Legendre L (2012) Numerical Ecolog, 3rd English edn. Elsevier Science BV, Amsterdam

    Google Scholar 

  • Linzmaier SM, Twardochleb LA, Olden JD, Mehner T, Arlinghaus R (2018) Size-dependent foraging niches of European Perch Perca fluviatilis (Linnaeus, 1758) and North American Yellow Perch Perca flavescens (Mitchill, 1814). Environ Biol Fish 101:23–37

    Article  Google Scholar 

  • MacArthur RH, Levins R (1967) The limiting similarity, convergence and divergence of coexisting species. Am Nat 101(921):377–385

    Article  Google Scholar 

  • Macpherson E (1981) Resource partitioning in a Mediterranean demersal fish community. Mar Ecol Prog Ser 4:183–193

    Article  Google Scholar 

  • Majluf P, De la Puente S, Christensen V (2017) The little fish that can feed the world. Fish Fish 18(4):772–777

    Article  Google Scholar 

  • Mavuti KM, Nyunja JA, Wakwabi EO (2004) Trophic ecology of some common juvenile fish species in Mtwapa Creek, Kenya. Western Indian Ocean J Mar Sci 3(2):179–187

    Google Scholar 

  • Mihalitsis M, Bellwood DR (2017) A morphological and functional basis for maximum prey size in piscivorous fishes. PLoS One 12(9):e0184679

    Article  Google Scholar 

  • Milton DA, Blaber SJM, Rawlinson NJF (1990) Diet and prey selection of six species of tuna baitfish in three coral reef lagoons in the Solomon Islands. J Fish Biol 37:205–224

    Article  Google Scholar 

  • Munk P (1997) Prey size spectra and prey availability of larval and small juvenile cod. J Fish Biol 51:340–351

    Article  Google Scholar 

  • Munroe TA, Nizinski M (1999) Engraulidae. Anchovies. In: Carpenter KE, Niem VH (eds) FAO species identification guide for fishery purposes. The living marine resources of the WCP, vol 3. Batoid fishes, chimaeras and bony fishes part 1 (Elopidae to Linophrynidae). FAO, Rome, pp 1698–1706

  • Munroe TA, Wongratana T, Nizinski MS (1999) Clupeidae. Herrings (also, sardines, shads, sprats, pilchards and menhadens). In Carpenter KE and Niem VH (eds) FAO species identification guide for fishery purposes. The living marine resources of the WCP, vol 3, Batoid fishes, chimaeras and bony fishes part 1 (Elopidae to Linophrynidae). FAO, Rome, pp 1775–1784

  • Nair KV (1998) Studies on the fishery, biology and population dynamics of anchovies of the Kerala coast. Dissertation, Mahatma Gandhi University

  • Nakamura Y, Horinouchi M, Nakai T, Sano M (2003) Food habits of fishes in a seagrass bed on a fringing coral reef at Iriomote Island, southern Japan. Ichthyol Res 50:15–22

    Article  Google Scholar 

  • Nelson JA, Stallings CD, Landing WM, Chanton J (2013) Biomass transfer subsidizes nitrogen to offshore food webs. Ecosystems 16(6):1130–1138

    Article  CAS  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2016) vegan: community ecology package. R package version 2.4-0. https://CRAN.R-project.org/package=vegan/. Accessed 14 Apr 2018

  • Olden JD, Poff NL, Bestgen KR (2006) Life-history strategies predict fish invasions and extirpations in the Colorado River Basin. Ecol Monogr 76(1):25–40

    Article  Google Scholar 

  • Pearre S (1986) Ratio-based trophic niche breadths of fish, the Sheldon spectrum, and the size-efficiency hypothesis. Mar Ecol Prog Ser 27:299–314

    Article  Google Scholar 

  • Pepin P, Penney RW (1997) Patterns of prey size and taxonomic composition in larval fish: are there general size-dependent models? J Fish Biol 51(Supplement A):84–100

    Article  Google Scholar 

  • Polis GA (1984) Age structure component of niche width and intraspecific resource partitioning: can age groups function as ecological species? Am Nat 123(4):541–564

    Article  Google Scholar 

  • Root RB (1967) The niche exploitation pattern of the blue-gray gnatcatcher. Ecol Monograph 37:317–350

    Article  Google Scholar 

  • Sabatés A, Saiz E (2000) Itra- and interspecific variability in prey size and niche breadth of myctophiform fish larvae. Mar Ecol Prog Ser 201:261–271

    Article  Google Scholar 

  • Salarpour A, Mohammad D, Behzadi S, Seraji F (2008) Reproduction and feeding of buccaneer anchovy (Encrasicholina punctifer) from coastal waters of Qeshm Island, the Persian Gulf. Iran Sci Fish J 17(1):45–54

    Google Scholar 

  • Scharf FS, Schlight KK (2000) Feeding habits of red drum (Scianops ocellatus) in Galveston Bay, Texas; seasonal diet variation and predator-prey size relationships. Estuaries 23(1):128–139

    Article  Google Scholar 

  • Scharf FS, Juanes F, Sutherland M (1998) Inferring ecological relationships from the edges of scatter diagrams: comparison of regression techniques. Ecology 79(2):448–460

    Article  Google Scholar 

  • 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 208:29–248

    Article  Google Scholar 

  • Schoener TW (2009) Ecological niche. In: Levin SA (ed) The princeton guide to ecology. Princeton University Press, New Jersey, pp 3–13

    Google Scholar 

  • Sheaves M, Baker R, Abrantes KG, Connolly RM (2016) Fish biomass in tropical estuaries: substantial variation in food web structure, sources of nutrition and ecosystem-supporting processes. Estuar Coast. https://doi.org/10.1007/s12237-016-0159-0

    Article  Google Scholar 

  • Somerfield PJ (2008) Identification of the Bray-Curtis similarity index: comment on Yoshioka (2008). Mar Ecol Prog Ser 372:303–306

    Article  Google Scholar 

  • Taher MM (2010) Specialization, trophic breadth and diet overlap of thirteen small marine fish species from Shatt Al-Basrah Canal, Southern Iraq. Marsh Bull 5(2):118–130

    Google Scholar 

  • Whitehead PJP, Nelson GJ, Wongratana T (1988) FAO species catalogue, clupeoid fishes of the world (suborder clupeoidei), vol 7. UNDP FAP, Rome

    Google Scholar 

Download references

Acknowledgements

We thank P. J. Hundt for helpful discussions, the 2013 Summer Institute in Taiwan staff, and our colleagues who assisted with fieldwork at National Chiayi University, Taiwan, Gao Zheng Aquaculture, Taiwan, James Cook University, Australia, the Museum and Art Gallery of the Northern Territory, Australia, and Rajamangala University of Technology Srivijaya, Thailand. We thank the reviewers for their suggestions that improved the quality of our manuscript. This work was funded in part by the Lerner-Gray Memorial Fund for Marine Research (American Museum of Natural History), Dayton Research Fund (Bell Museum of Natural History, University of Minnesota), the Minnesota Agricultural Experiment Station, and the East Asia and Pacific Summer Institutes Program from the National Science Council of Taiwan and the National Science Foundation, USA (1316912). During the preparation of this manuscript J. P. E. received financial support from a National Science Foundation Graduate Research Fellowship (00039202).

Author information

Authors and Affiliations

  1. Conservation Sciences Graduate Program, University of Minnesota, 135B Skok Hall, 2003 Upper Buford Circle, St. Paul, MN, 55108, USA

    Joshua P. Egan

  2. Bell Museum of Natural History, University of Minnesota, 100 Ecology, 1987 Upper Buford Circle, St. Paul, MN, 55108, USA

    Joshua P. Egan & Andrew M. Simons

  3. Department of Fisheries, Wildlife and Conservation Biology, University of Minnesota, 135B Skok Hall, 2003 Upper Buford Circle, St. Paul, MN, 55108, USA

    Sean Gibbs & Andrew M. Simons

Authors
  1. Joshua P. Egan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sean Gibbs
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrew M. Simons
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joshua P. Egan.

Ethics declarations

Conflict of interest

The authors declare they have no conflict of interest.

Human and animal rights

The authors followed all relevant international, national, and institutional guidelines for the care and use of fishes. Research was conducted according to animal care and use protocol 1304-30541A approved by the University of Minnesota Animal Care and Use Committee.

Additional information

Responsible Editor: E. Hunter.

Reviewed by Undisclosed experts.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 79 kb)

Supplementary material 2 (PDF 1291 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Egan, J.P., Gibbs, S. & Simons, A.M. Trophic niches through ontogeny in 12 species of Indo-Pacific marine Clupeoidei (herrings, sardines, and anchovies). Mar Biol 165, 153 (2018). https://doi.org/10.1007/s00227-018-3410-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-018-3410-3

Search

Navigation