Skip to main content
Log in

Forage fish to growing chicks: shared food resources between two closely related tern species

Marine Biology Aims and scope Submit manuscript

Abstract

The assessment of the relevance of forage fish in seabird diet and how different species partition food resources is fundamental to understand predator–prey relationships. We assessed the importance of forage fish in the diet of Royal (Thalasseus maximus maximus) and Cayenne (T. sandvicensis eurygnathus) terns and their partitioning of food resources during the early and late chick stages of 2013 and 2014 at a colony in Argentina. Direct observation of prey deliveries during chick provisioning showed that diet composition of Royal and Cayenne terns comprised at least 16 and 9 prey species, respectively. In both tern species, Argentine Anchovy (Engraulis anchoita) and five species of silversides (Odontesthes spp.) were the main prey fed to chicks (over 90% contribution, anchovy and silversides pooled). Both tern species fed their chicks with similar prey species, but Royal terns delivered, in general, larger prey than Cayenne terns. Based on carbon and nitrogen isotopic values from chick whole blood samples, Bayesian mixing models showed that anchovies and silversides contributed similarly to the diet of both tern species’ chicks. Both conventional and stable isotope methods showed a high overlap in their trophic niches. Prey sizes delivered to chicks were larger in the late chick stage and the second study season. Wind speed did not have a significant effect on the frequency of the different prey species and sizes delivered to chicks by both tern species. As anchovies and silversides are fishery targets, tern trophic requirements should be considered when planning future fisheries development and management.

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

Access this article

Price includes VAT (Finland)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  • Agresti A (2002) Categorical data analysis. John Wiley AND Sons Inc., New Jersey

    Book  Google Scholar 

  • Ashmole NP, Ashmole MJ (1967) Comparative feeding ecology of seabirds of a tropical oceanic island, vol 24. Peabody Museum of Natural History, Yale University Bulletin, New Haven, pp 1–131

    Google Scholar 

  • Barger CP, Kitaysky AS (2011) Isotopic segregation between sympatric seabird species increases with nutritional stress. Biol Lett 8:442–445. https://doi.org/10.1098/rsbl.2011.1020

    Article  PubMed  PubMed Central  Google Scholar 

  • Barger CP, Young RC, Will A, Ito M, Kitaysky AS (2016) Resource partitioning between sympatric seabird species increases during chick-rearing. Ecosphere 7:e01447. https://doi.org/10.1002/ecs2.1447

    Article  Google Scholar 

  • Barrett RT, Camphuysen CJ, Anker-Nilssen T, Chardine JW, Furness RW, Garthe S, Hüppop O, Leopold MF, Montevecchi WA, Veit RR (2007) Diet studies of seabirds: a review and recommendations. ICES J Mar Sci 64:1675–1691. https://doi.org/10.1093/icesjms/fsm152

    Article  Google Scholar 

  • Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451–458. https://doi.org/10.1086/342800

    Article  CAS  PubMed  Google Scholar 

  • Bodey TW, Ward EJ, Phillips RA, McGill RAR, Bearhop S (2014) Species versus guild level differentiation revealed across the annual cycle by isotopic niche examination. J Anim Ecol 83:470–478. https://doi.org/10.1111/1365-2656.12156

    Article  PubMed  Google Scholar 

  • Bond AL, Diamond AW (2011) Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl 21:1017–1023. https://doi.org/10.1890/09-2409.1

    Article  PubMed  Google Scholar 

  • Bovcon N (2016) Evaluación de las pesquerías recreativas costeras de la Provincia del Chubut, Argentina: base para su ordenamiento y manejo. Doctoral thesis, Universidad Nacional del Comahue

  • Buckley PA, Buckley FG (2002) Royal tern (Sterna maxima). In: Rodewald PG (ed) The birds of North America. Cornell Lab of Ornithology, Ithaca

    Google Scholar 

  • Bugoni L, McGill RAR, Furness RW (2008) Effects of preservation methods on stable isotope signatures in bird tissues. Rapid Commun Mass Sp 22:2457–2462. https://doi.org/10.1002/rcm.3633

    Article  CAS  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information theoretic approach. Springer-Verlag, New York

    Google Scholar 

  • Cezilly F, Wallace J (1988) The determination of prey captured by birds through direct field observations: a test of the method. Colon Waterbirds 11:110–112. https://doi.org/10.2307/1521177

    Article  Google Scholar 

  • Chao LN, Pereira LE, Vieira JP (1985) Estuarine fish community of the dos Patos Lagoon, Brazil: a baseline study. In: Yañez Arancibia A (ed) Fish community ecology in estuaries and coastal lagoons: towards an ecosystem integration. DR(R) UNAM Press, México, pp 429–450

    Google Scholar 

  • Ciechomski JD (1981) Ictioplancton. In: Boltovskoy D (ed) Atlas del Zooplancton del Atlántico Sudoccidental y métodos de trabajo con el zooplancton marino. Instituto Nacional de Investigación y Desarrollo Pesquero, Mar de Plata, pp 829–935

    Google Scholar 

  • Crawford RJM, Dyer BM (1995) Responses by four seabird species to a fluctuating availability of Cape Anchovy Engraulis capensis off South Africa. Ibis 137:329–339. https://doi.org/10.1111/j.1474-919X.1995.tb08029.x

    Article  Google Scholar 

  • Croxall JP, Prince PA, Reid K (1997) Dietary segregation of krill-eating South Georgia seabirds. J Zool 242:531–556. https://doi.org/10.1111/j.1469-7998.1997.tb03854.x

    Article  Google Scholar 

  • Cury PM, Boyd IL, Bonhommeau S, Anker-Nilssen T, Crawford RJ, Furness RW, Mills JA, Murphy EJ, Osterblom H, Paleczny M, Piatt JF, Roux JP, Shannon L, Sydeman WJ (2011) Global seabird response to forage fish depletion-one third for the birds. Science 334:1703–1706. https://doi.org/10.1126/science.1212928

    Article  CAS  PubMed  Google Scholar 

  • Diaz MV (2010) Análisis espacio-temporal del estado nutricional de larvas de anchoíta Engraulis anchoita. Relación con las características hidrográficas y la disponibilidad de alimento. Doctoral thesis, Universidad de Buenos Aires

  • Faraway JJ (2006) Extending the linear model with R: generalized linear, mixed effects and nonparametric regression models. Chapman and Hall and CRC Press, Boca Raton

    Google Scholar 

  • Fasola M, Bogliani G, Saino N, Canova L (1989) Foraging, feeding and time activity niches of eight species of breeding seabirds in the coastal wetlands of the Adriatic Sea. B Zool 56:61–72. https://doi.org/10.1080/11250008909355623

    Article  Google Scholar 

  • Fernández Ajó AA, Gatto A, Yorio P (2011) Patterns of prey provisioning in relation to chick age in the South American tern (Sterna hirundinacea). Ornitol Neotrop 22:361–368

    Google Scholar 

  • Fracasso HAA, Branco JO, Barbieri E (2011) A comparison of foraging between the South American and Cabot’s tern in southern Brazil. Biota Neotrop 11:189–196. https://doi.org/10.1590/S1676-06032011000300016

    Article  Google Scholar 

  • Furness RW, Tasker ML (2000) Seabird-fishery interactions: quantifying the sensitivity of seabirds to reductions in sandeel abundance, and identification of key areas for sensitive seabirds in the North Sea. Mar Ecol Prog Ser 202:253–264. https://doi.org/10.3354/meps202253

    Article  Google Scholar 

  • Gaglio D, Cook TR, Connan M, Ryan PG, Sherley RB (2016) Dietary studies in birds: testing a non-invasive method using digital photography in seabirds. Method Ecol Evol 8:214–222. https://doi.org/10.1111/2041-210X.12643

    Article  Google Scholar 

  • Garciarena DA, Buratti C (2013) Pesca Comercial de Anchoíta Bonaerense (Engraulis anchoita) entre 1993 y 2011. Rev Invest y Des Pesq 23:87–106

    Google Scholar 

  • Gatto AJ, Yorio P (2009) Provisioning of mates and chicks by Cayenne and Royal terns: resource partitioning in northern Patagonia, Argentina. Emu 109:49–55. https://doi.org/10.1071/MU08025

    Article  Google Scholar 

  • Gatto AJ, Yorio P (2016) Assessing the trophic niche of South American terns integrating conventional and isotopic methods. Emu 116:230–240. https://doi.org/10.1071/MU15010

    Article  Google Scholar 

  • Greenstreet SPR, Fraser HM, Piet GJ (2009) Using MPAs to address regional-scale ecological objectives in the North Sea: modelling the effects of fishing effort displacement. ICES J Mar Sci 66:90–100. https://doi.org/10.1093/icesjms/fsn214

    Article  Google Scholar 

  • Hansen JE, Martos P, Madirolas A (2001) Relationship between spatial distribution of the Patagonian stock of Argentine Anchovy, Engraulis anchoita, and sea temperatures during late spring to early summer. Fish Oceanogr 10:193–206. https://doi.org/10.1046/j.1365-2419.2001.00166.x

    Article  Google Scholar 

  • Hilborn R, Amoroso RO, Bogazzi E, Jensen OP, Parma AM, Szuwalski C, Walters CJ (2017) When does fishing forage species affect their predators? Fish Res 191:211–221. https://doi.org/10.1016/j.fishres.2017.01.008

    Article  Google Scholar 

  • Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188. https://doi.org/10.2307/1368807

    Article  Google Scholar 

  • Hobson KA, Gibbs HL, Gloutney ML (1997) Preservation of blood and tissue samples for stable-carbon and stable-nitrogen isotopes analysis. Can J Zool 75:1720–1723. https://doi.org/10.1139/z97-799

    Article  CAS  Google Scholar 

  • Hulsman K (1981) Width of gape as a determinant of size of prey eaten by terns. Emu 81:29–32. https://doi.org/10.1071/MU9760143

    Article  Google Scholar 

  • Hulsman K (1988) The structure of seabird communities: an example from Australian waters. In: Burger J (ed) Seabirds and other marine vertebrates: competition, predation, and other interactions. Columbia University Press, New York, pp 59–91

    Google Scholar 

  • Irigoyen A, Trobbiani G, Casalinuovo M, Alonso M et al (2018) Peces y pesca deportiva Argentina, Mar y Patagonia. Remitente Patagonia, Trelew

    Google Scholar 

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

    Article  Google Scholar 

  • Jackson MC, Donohue I, Jackson AL, Britton JR, Harper DM, Grey J (2012) Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology. PLoS One 7:e31757. https://doi.org/10.1371/journal.pone.0031757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karnovsky NJ, Hobson KA, Iverson SJ (2012) From lavage to lipids: estimating diets of seabirds. Mar Ecol Prog Ser 451:263–284. https://doi.org/10.3354/meps09713

    Article  CAS  Google Scholar 

  • Krebs CJ (1999) Ecological methodology. Benjamin Cummings/Addison-Wesley Educational Publishers Inc., Menlo Park

    Google Scholar 

  • Larson K, Craig D (2006) Digiscoping vouchers for diet studies in bill-load holding birds. Waterbirds 29:198–202

    Article  Google Scholar 

  • Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88:42–48. https://doi.org/10.1890/0012-9658(2007)88%5b42:CSIRPF%5d2.0.CO;2

    Article  PubMed  Google Scholar 

  • Lenzi J, Jiménez S, Caballero-Sadi D, Alfaro M, Laporta P (2010) Some aspects of the breeding biology of Royal (Thalasseus maximus) and Cayenne terns (T. sandvicensis eurygnathus) on Isla Verde, Uruguay. Ornitol Neotrop 21:361–370

    Google Scholar 

  • Liechty JS, Fontenot QC, Pierce AR (2016) Diet composition of Royal tern (Thalasseus maximus) and Sandwich tern (T. sandvicensis) at Isles Dernieres Barrier Island Refuge, Louisiana. Waterbirds 39:58–68. https://doi.org/10.1675/063.039.0107

    Article  Google Scholar 

  • Lisnizer N, Cotichelli L, Yorio P, Basso N, Gatto A (2014) Using morphometry and molecular markers for sexing South American, Cayenne and Royal terns breeding in Patagonia, Argentina. Waterbirds 37:183–190. https://doi.org/10.1675/063.037.0207

    Article  Google Scholar 

  • Llompart FM (2011) La ictiofauna de Bahía San Blas (Provincia de Buenos Aires) y su relación con la dinámica de las pesquerías deportiva y artesanal. Doctoral thesis, Universidad Nacional de la Plata

  • Llompart FM, Colautti DC, Baigún CRM (2012) Assessment of a major shore-based marine recreational fishery in the southwest Atlantic, Argentina. New Zeal J Mar Fresh 46:1–14. https://doi.org/10.1080/00288330.2011.595420

    Article  Google Scholar 

  • Mancini PLM, Hobson KA, Bugoni L (2014) The role of body size in shaping the trophic structure of tropical seabird communities. Mar Ecol Prog Ser 497:243–257. https://doi.org/10.3354/meps10589

    Article  Google Scholar 

  • McGinnis TW, Emslie SD (2001) The foraging ecology of Royal and Sandwich terns in North Carolina, USA. Waterbirds 24:361–370. https://doi.org/10.2307/1522066

    Article  Google Scholar 

  • McLeay LJ, Page B, Goldsworthy SD, Ward TM, Paton DC (2009) Size matters: variation in the diet of chick and adult Crested terns. Mar Biol 156:1765–1780

    Article  Google Scholar 

  • Menni RC, Ringuelet RA, Aramburu RH (1984) Peces Marinos de Argentina y Uruguay. Editorial Hemisferio Sur, Buenos Aires

    Google Scholar 

  • Orians GH, Pearson NE (1979) On the theory of central place foraging. In: Horn DJ, Stairs GR, Mitchelle RG (eds) Analysis of ecological systems. Ohio State University Press, Columbus, pp 155–177

    Google Scholar 

  • Paiva VH, Ramos JA, Catry T, Pedro P, Medeiros R, Palma J (2006) Influence of environmental factors and energetic value of food on little tern Sterna albifrons chick growth and food delivery. Bird Study 53:1–11. https://doi.org/10.1080/00063650609461410

    Article  Google Scholar 

  • Parnell AC, Phillips DL, Bearhop S, Semmens BX, Ward EJ, Moore JW, Jackson AL, Grey J, Kelly DJ, Inger R (2013) Bayesian stable isotope mixing models. Environmetrics 24:387–399. https://doi.org/10.1002/env.2221

    Article  Google Scholar 

  • Pereira JC, Ramos JA (2009) Subtropical Roseate terns (Sterna dougallii) of Santa Maria (Azores) deliver more appropriate sized prey to their chicks than Common terns (Sterna hirundo). Airo 19:3–12

    Google Scholar 

  • Pikitch E, Boersma PD, Boyd IL, Conover DO, Cury P, Essington T, Heppell SS, Houde ED, Mangel M, Pauly D, Plagányi E, Sainsbury K, Steneck RS (2012) Little fish, big impact: managing a crucial link in ocean food webs. Lenfest Ocean Program, Washington, DC

    Google Scholar 

  • Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods, and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189. https://doi.org/10.1007/s00442-006-0630-x

    Article  PubMed  Google Scholar 

  • Quintana F, Yorio P (1997) Breeding biology of Royal (Sterna maxima) and Cayenne (S. eurygnatha) terns at Punta León, Chubut. Wilson Bull 109:650–662

    Google Scholar 

  • Ramos JA, Pedro P, Matos A, Paiva VH (2013) Relation between climatic factors, diet and reproductive parameters of Little terns over a decade. Acta Oecol 53:56–62. https://doi.org/10.1016/j.actao.2013.09.001

    Article  Google Scholar 

  • Ricklefs RE, White SC (1981) Growth and energetics of chicks of the Sooty tern (Sterna fuscata) and Common tern (S. hirundo). Auk 98:361–378. https://doi.org/10.1093/auk/98.2.361

    Article  Google Scholar 

  • Ridoux V (1994) The diets and dietary segregation of seabirds at the subantarctic Crozet Islands. Mar Ornithol 22:1–192

    Google Scholar 

  • Robertson GS, Bolton M, Grecian WJ, Wilson LJ, Davies W, Monaghan P (2014) Resource partitioning in three congeneric sympatrically breeding seabirds: foraging areas and prey utilization. Auk 131:434–446. https://doi.org/10.1642/AUK-13-243.1

    Article  Google Scholar 

  • Shealer DA (1998) Size-selective predation by a specialist forager, the Roseate tern. Auk 115:519–525. https://doi.org/10.2307/4089217

    Article  Google Scholar 

  • Shealer D, Liechty JS, Pierce AR, Pyle P, Patten MA (2016) Sandwich tern (Thalasseus sandvicensis), version 3.0. In: Rodewald PG (ed) The birds of North America. Cornell Lab of Ornithology, Ithaca

    Google Scholar 

  • Smith JA, Mazumder D, Suthers IM, Taylor MD (2013) To fit or not to fit: evaluating stable isotope mixing models using simulated mixing polygons. Meth Ecol Evol 4:612–618. https://doi.org/10.1111/2041-210X.12048

    Article  Google Scholar 

  • Stienen EWM, Van Beers PWM, Brenninkmeijer A, Habraken JMPM, Raaijmakers MHJE, Van Tienen PGM (2000) Reflections of a specialist: patterns in food provisioning and foraging conditions in Sandwich terns Sterna sandvicensis. Ardea 88:33–49

    Google Scholar 

  • Suárez N, Marinao C, Kasinsky T, Yorio P (2014) Distribución reproductiva y abundancia de gaviotas y gaviotines en el Área Natural Protegida Bahía San Blas, Buenos Aires. Hornero 29:29–36

    Google Scholar 

  • Thomson JA, Heithaus MR, Burkholder DA, Vaudo JJ, Wirsing AJ, Dill LM (2012) Site specialists, diet generalists? Isotopic variation, site fidelity, and foraging by Loggerhead Turtles in Shark Bay, Western Australia. Mar Ecol Prog Ser 453:213–226

    Article  Google Scholar 

  • Turner TF, Collyer ML, Krabbenhoft TJ (2010) A general hypothesis testing framework for stable isotope ratios in ecological studies. Ecology 91:2227–2233. https://doi.org/10.1890/09-1454.1

    Article  PubMed  Google Scholar 

  • Velarde E, Ezcurra E, Anderson D (2013) Seabird diets provide early warning of sardine fishery declines in the Gulf of California. Sci Rep 3:1332

    Article  CAS  Google Scholar 

  • Wambach EJ, Emslie SD (2003) Seasonal and annual variation in the diet of breeding, know-age Royal terns in North Carolina. Wilson Bull 115:448–454

    Article  Google Scholar 

  • Wiens JA (1989) The ecology of bird communities, Vol. 1. Foundations and patterns. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Yorio P, Efe M (2008) Population status of Royal and Cayenne terns breeding in Argentina and Brazil. Waterbirds 31:561–570. https://doi.org/10.1675/1524-4695-31.4.561

    Article  Google Scholar 

  • Zalba SM, Nebbia AJ, Fiori SM (2008) Propuesta de Plan de Manejo de la Reserva Natural de Uso Múltiple Bahía San Blas. Universidad Nacional del Sur, Bahía Blanca

    Google Scholar 

Download references

Acknowledgements

Thanks to Centro para el Estudio de Sistemas Marinos (CCT CONICET-CENPAT) for institutional support and Dirección de Administración de Áreas Protegidas, Ministerio de Asuntos Agrarios Provincia de Buenos Aires for the permits to conduct the research at the Bahía San Blas protected area. Thanks to N. Bovcon and D. Figueroa for help in the determination of prey species, O. Frumento for help in data analysis, and T. Kasinsky for her help in fieldwork.

Funding

This study was funded by Wildlife Conservation Society and Consejo Nacional de Investigaciones Científicas y Técnicas (Project PIP no. 112 01 01061).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cristian Marinao.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

Animal handling and feather sampling were permitted under appropriate permits (DISPOSICIÓN no 201/12 Dirección de Administración de Áreas Protegidas-Ministerio de Asuntos Agrarios of Buenos Aires Province, Argentina). All applicable international, national, and institutional guidelines for the care and use of animals were followed.

Additional information

Responsible Editor: V. H. Paiva.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Reviewed by D. Gaglio and undisclosed experts.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Marinao, C., Suárez, N., Gatto, A. et al. Forage fish to growing chicks: shared food resources between two closely related tern species. Mar Biol 166, 121 (2019). https://doi.org/10.1007/s00227-019-3570-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-019-3570-9

Navigation