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.



References
Agresti A (2002) Categorical data analysis. John Wiley AND Sons Inc., New Jersey
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
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
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
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
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
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
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
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
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
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information theoretic approach. Springer-Verlag, New York
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
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
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
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
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
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
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
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
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
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
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
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
Garciarena DA, Buratti C (2013) Pesca Comercial de Anchoíta Bonaerense (Engraulis anchoita) entre 1993 y 2011. Rev Invest y Des Pesq 23:87–106
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
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
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
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
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
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
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
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
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
Irigoyen A, Trobbiani G, Casalinuovo M, Alonso M et al (2018) Peces y pesca deportiva Argentina, Mar y Patagonia. Remitente Patagonia, Trelew
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
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
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
Krebs CJ (1999) Ecological methodology. Benjamin Cummings/Addison-Wesley Educational Publishers Inc., Menlo Park
Larson K, Craig D (2006) Digiscoping vouchers for diet studies in bill-load holding birds. Waterbirds 29:198–202
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
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
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
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
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
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
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
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
Menni RC, Ringuelet RA, Aramburu RH (1984) Peces Marinos de Argentina y Uruguay. Editorial Hemisferio Sur, Buenos Aires
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
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
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
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
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
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
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
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
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
Ridoux V (1994) The diets and dietary segregation of seabirds at the subantarctic Crozet Islands. Mar Ornithol 22:1–192
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
Shealer DA (1998) Size-selective predation by a specialist forager, the Roseate tern. Auk 115:519–525. https://doi.org/10.2307/4089217
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
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
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
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
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
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
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
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
Wiens JA (1989) The ecology of bird communities, Vol. 1. Foundations and patterns. Cambridge University Press, Cambridge
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
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
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.
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This study was funded by Wildlife Conservation Society and Consejo Nacional de Investigaciones Científicas y Técnicas (Project PIP no. 112 01 01061).
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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.
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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
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DOI: https://doi.org/10.1007/s00227-019-3570-9