Skip to main content

Advertisement

SpringerLink
Log in

Diet of adult and immature imperial cormorants, Leucocarbo atriceps, from southern Patagonia. A combined dietary approach and an exploratory analysis of stable isotopes of pellet membrane

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

Abstract

The use of combined conventional and stable isotope analyses (SIA) to study the diet of seabirds has become very frequent. Unfortunately, information on the trophic ecology of immature seabirds remains scarce because the sampling of tissues to perform SIA is often very limited due to the difficulty to capture these birds. The koilin membrane, which covers the regurgitated pellet casts of some seabirds, could offer an interesting non-intrusive alternative tissue to perform SIA. In this two-year study of the diet of imperial cormorants in southern Patagonia, we (1) compare the diets of breeding and non-breeding birds through conventional pellet analysis; (2) describe the diet of breeding adults and chicks through a combined method of pellet analysis and whole blood SIA; and finally, (3) compare SIA values of breeding adults obtained from blood with those obtained from koilin membranes. We found that immature individuals incorporated abundant invertebrate taxons, compared with breeding adults which relied mainly on fish. Younger and inexperienced individuals, which are not under the constraint to feed chicks, are feeding on more predictable, but lower trophic and less energetic prey. By comparing the stable isotope values of koilin and blood in breeding adults, a correlated interannual difference between the two seasons was found. Under the light of our results, the koilin offers an encouraging alternative to blood in the study of trophic ecology, particularly for ages or stages in which capture is not possible.

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

  • Barrett RT, Camphuysen K, Anker-Nilssen T et al (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 

  • Barrionuevo M, Ciancio J, Marchisio N, Frere E (2018) Parental body condition and high energy value of fish determine nestling success in Magellanic penguin (Spheniscus magellanicus). Mar Biol 165:105. https://doi.org/10.1007/s00227-018-3358-3

    Article  Google Scholar 

  • Bond AL, Jones IL (2009) A practical introduction to stable-isotope analysis for seabird biologists: approaches, cautions and caveats. Mar Ornithol 37:183–188

    Google Scholar 

  • Boschi E, Fischbach C, Iorio M (1992) Catálogo ilustrado de los crustáceos estomatópodos y decápodos marinos de Argentina. Frente Marítimo 10:7–94

    Google Scholar 

  • Bulgarella M, Pizarro LC, Quintana F et al (2008) Diet of imperial cormorants (Phalacrocorax atriceps) and rock shags (P. Magellanicus) breeding sympatrically in Patagonia. Argentina Ornitol Neotrop 19:553–563

    Google Scholar 

  • Campioni L, Granadeiro JP, Catry P (2016) Niche segregation between immature and adult seabirds: does progressive maturation play a role? Behav Ecol 27:426–433. https://doi.org/10.1093/beheco/arv167

    Article  Google Scholar 

  • Carscadden JE, Montevecchi WA, Davoren GK, Nakashima BS (2002) Trophic relationships among capelin (Mallotus villosus) and seabirds in a changing ecosystem. ICES J Mar Sci 59:1027–1033

    Article  Google Scholar 

  • Chiaradia A, Forero MG, Hobson KA, Swearer SE, Hume F, Renwick L, Dann P (2012) Diet segregation between two colonies of little penguins Eudyptula minor in southeast Australia. Austral Ecol 37:610–619. https://doi.org/10.1111/j.1442-9993.2011.02323.x

    Article  Google Scholar 

  • Ciancio JE, Pascual M, Beauchamp D (2007) Energy density of Patagonian aquatic organisms and empirical predictions based on water content. Trans Am Fish Soc 136:1415–1422. https://doi.org/10.1577/T06-173.1

    Article  Google Scholar 

  • Ciancio JE, Righi C, Faiella A, Frere E (2016) Blood-specific isotopic discrimination factors in the Magellanic penguin (Spheniscus magellanicus). Rapid Commun Mass Spectrom 30:1865–1869. https://doi.org/10.1002/rcm.7661

    Article  CAS  PubMed  Google Scholar 

  • Craig EC, Dorr BS, Hanson-Dorr KC, Sparks JP, Curtis PD (2015) Isotopic discrimination in the double-crested cormorant (Phalacrocorax auritus). PLoS One 10:1–7

    Article  Google Scholar 

  • Daunt F, Afanasyev V, Adam A, Croxall JP, Wanless S (2007) From cradle to early grave: juvenile mortality in European shags Phalacrocorax aristotelis results from inadequate development of foraging proficiency. Biol Lett 3:371–374. https://doi.org/10.1098/rsbl.2007.0157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez SJ, Yorio P, Ciancio JE (2019) Diet composition of expanding breeding populations of the Magellanic Penguin. Mar Biol Res 15:84–96. https://doi.org/10.1080/17451000.2019.1596286

    Article  Google Scholar 

  • Ferrari S, Alegre B, Gandini P (2004) Dieta del cormorán imperial (Phalacrocorax atriceps) en el sur de Santa Cruz (Patagonia, Argentina). Ornitol Neotrop 15:103–110

    Google Scholar 

  • Forero MG, Hobson KA, Bortolotti GR, Donázar JA, Bertellotti M, Blanco G (2002) Food resource utilisation by the Magellanic penguin evaluated through stable-isotope analysis: segregation by sex and age and influence on offspring quality. Mar Ecol Prog Ser 234:289–299

    Article  Google Scholar 

  • Frere E, Gandini P, Lichtschein V (1996) Variación latitudinal en la dieta del pingüino de Magallanes (Spheniscus magellanicus) en la costa patagónica, Argentina. Ornitol Neotrop 7:35–41

    Google Scholar 

  • Frere E, Quintana F, Gandini P (2005) Cormoranes de la costa patagónica: estado poblacional, ecología y conservación. Hornero 20:35–52

    Google Scholar 

  • Gómez Laich A, Quintana F, Shepard ELC, Wilson RP (2012) Intersexual differences in the diving behaviour of imperial cormorants. J Ornithol 153:139–147. https://doi.org/10.1007/s10336-011-0714-1

    Article  Google Scholar 

  • Gosztonyi AE, Kuba L (1996) Atlas de huesos craneales y de la cintura escapular de peces costeros patagónicos. Fund Patagon Nat Inf Técnico 4:1–29

    Google Scholar 

  • Harris S, Sáenz Samaniego RA, Raya Rey A (2016) Insights into diet and foraging behavior of Imperial Shags ( Phalacrocorax atriceps) breeding at Staten and Becasses islands, Tierra del Fuego, Argentina. Wilson J Ornithol 128:811–820. https://doi.org/10.1676/15-141.1

    Article  Google Scholar 

  • Healy K, Guillerme T, Kelly SB, Inger R, Bearhop S, Jackson AL (2018) SIDER: an R package for predicting trophic discrimination factors of consumers based on their ecology and phylogenetic relatedness. Ecography 41:1393–1400. https://doi.org/10.1111/ecog.03371

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ibarra C, Marinao C, Suárez N, Yorio P (2018) Differences between colonies and chick-rearing stages in imperial cormorant (Phalacrocorax atriceps) diet composition: implications for trophic studies and monitoring. Wilson J Ornithol 130:224–234. https://doi.org/10.1676/16-184.1

    Article  Google Scholar 

  • Jaeger A, Goutte A, Lecomte VJ, Richard P, Chastel O, Barbraud C, Weimerskirch H, Cherel Y (2014) Age, sex, and breeding status shape a complex foraging pattern in an extremely long-lived seabird. Ecology 95:2324–2333. https://doi.org/10.1890/13-1376.1

    Article  PubMed  Google Scholar 

  • Karnovsky NJ, Hobson KA, Iverson S, Hunt GL Jr (2008) Seasonal changes in diets of seabirds in the north water polynya: a multiple-indicator approach. Mar Ecol Prog Ser 357:291–299. https://doi.org/10.3354/meps07295

    Article  Google Scholar 

  • Kim HK, Choi CY, Jeong MS, Kang HY, Lee WS (2016) Regurgitation of the koilin layer in chinstrap penguins (Pygoscelis antarcticus) and its association with gastric parasites. Polar Res 35:25966. https://doi.org/10.3402/polar.v35.25966

    Article  Google Scholar 

  • Koen Alonso M, Crespo EA, Pedraza SN, Garcia NA, Coscarella MA (2000) Food habits of the South American sea lion, Otaria flavescens, off Patagonia, Argentina. Fish Bull 98:250–263

    Google Scholar 

  • Layman CA, Araujo MS, Boucek R et al (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol Rev 87:545–562. https://doi.org/10.1111/j.1469-185X.2011.00208.x

    Article  PubMed  Google Scholar 

  • Lombarte A, Rucabado J, Matallanas J, Lloris D (1991) Taxonomía numérica de Nototheniidae en base a la forma de los otolitos. Sci Mar 55:413–418

    Google Scholar 

  • Malacalza VE, Poretti TI, Bertellotti NM (1994) La dieta de Phalacrocorax albiventer en Punta Leon (Chubut, Argentina) durante la temporada reproductiva. Ornitol Neotrop 5:91–97

    Google Scholar 

  • Marshall AJ (2013) Biology and comparative physiology of birds, vol I. Academic Press, Cambridge

    Google Scholar 

  • Michalik A, Van Noordwijk HJ, Brickle P, Eggers T, Quillfeldt P (2010) The diet of the Imperial Shag Phalacrocorax atriceps at a colony on New Island, Falkland/Malvinas Islands combining different sampling techniques. Polar Biol 33:1537–1546. https://doi.org/10.1007/s00300-010-0843-7

    Article  Google Scholar 

  • Michalik A, McGill RA, Van Noordwijk HJ, Masello JF, Furness RW, Eggers T, Quillfeldt P (2013) Stable isotopes reveal variable foraging behaviour in a colony of the Imperial Shag Phalacrocorax atriceps: differences between ages, sexes and years. J Ornithol 154:239–249. https://doi.org/10.1007/s10336-012-0890-7

    Article  Google Scholar 

  • Millones A, Frere E, Gandini P (2005) Dieta del cormorán gris (Phalacrocorax gaimardi) en la Ría Deseado, Santa Cruz, Argentina. Ornitol Neotrop 16:519–527

    Google Scholar 

  • Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11:470–480. https://doi.org/10.1111/j.1461-0248.2008.01163.x

    Article  PubMed  Google Scholar 

  • Morgenthaler A (2019) El uso de los recursos tróficos de cuatro especies simpátricas de cormoranes (Phalacrocorax gaimardi, P. magellanicus, P. brasilianus y P. atriceps) en la Ría Deseado, Provincia de Santa Cruz. Dissertation, Universidad Nacional del Comahue, Argentina. https://doi.org/10.1007/s00300-022-03086-5

  • Morgenthaler A, Millones A, Gandini P, Frere E (2016) Pelagic or benthic prey? Combining trophic analyses to infer the diet of a breeding South American seabird, the red-legged cormorant, Phalacrocorax gaimardi. Emu 116:360–369. https://doi.org/10.1071/MU15101

    Article  Google Scholar 

  • Morgenthaler A, Millones A, Gandini P, Frere E (2020) The diet of adult and chick rock shags (Phalacrocorax magellanicus) inferred from combined pellet and stable isotope analyses. Polar Biol 43:511–521. https://doi.org/10.1007/s00300-020-02653-y

    Article  Google Scholar 

  • Morgenthaler A, Millones A, Gandini P, Frere E (2021) Which trophic discrimination factors fit the best? A combined dietary study of a coastal seabird. J Ornithol 162:179–190. https://doi.org/10.1007/s10336-020-01813-5

    Article  Google Scholar 

  • Morrison ML, Slack RD, Shanley E Jr (1978) Age and foraging ability relationships of olivaceous cormorants. Wilson Bull 1978:414–422

    Google Scholar 

  • Oksanen J, Blanchet F, Kindt R, et al (2016) Vegan: community ecology package. R package 2.3-3

  • Parnell AC, Inger R (2016). Simmr: a stable isotope mixing model. R Package version 0.4.1.

  • Piacentino GLM (1999) Osteología craneana de Odontesthes nigricans (RICHARDSON 1845) y Odontesthes smitii (LAHILLE 1929) de la ria de Puerto Deseado (Santa Cruz, Argentina) (Teleostei, Atherinopsidae). Boletim do Lab de Hidrobiol 12(1):1999

    Google Scholar 

  • Pineda S, Aubone A, Brunetti N (1996) Identificación y morfometría de las mandibulas de Loligo gahi y Loligo sanpaulensis (Cephalopoda, Loliginidae) del Atlántico Sudoccidental. Rev Investig y Desarro Pesq 10:85–99

    Google Scholar 

  • Polito MJ, Fisher S, Tobias CR, Emslie SD (2009) Tissue-specific isotopic discrimination factors in gentoo penguin (Pygoscelis papua) egg components: implications for dietary reconstruction using stable isotopes. J Exp Mar Biol Ecol 372:106–112. https://doi.org/10.1016/j.jembe.2009.02.014

    Article  CAS  Google Scholar 

  • Punta GE, Saravia JRC, Yorio PM (1993) The diet and foraging behaviour of two Patagonian cormorants. Mar Ornithol 21:27–36

    Google Scholar 

  • Punta G, Yorio P, Herrera G (2003) Temporal patterns in the diet and food partitioning in imperial cormorants (Phalacrocorax atriceps) and rock shags (P. magellanicus) breeding at Bahia Bustamante. Argentina Wilson Bull 115:307–315. https://doi.org/10.1676/02-119

    Article  Google Scholar 

  • Quillfeldt P, McGill RA, Masello JF, Poisbleau M, Van Noordwijk H, Demongin L, Furness RW (2009) Differences in the stable isotope signatures of seabird egg membrane and albumen–implications for non-invasive studies. Rapid Commun Mass Spectrom 23:3632–3636. https://doi.org/10.1002/rcm.4286

    Article  CAS  PubMed  Google Scholar 

  • Quillfeldt P, Schroff S, van Noordwijk HJ, Michalik A, Ludynia K, Masello JF (2011) Flexible foraging behaviour of a sexually dimorphic seabird: large males do not always dive deep. Mar Ecol Prog Ser 428:271–287. https://doi.org/10.3354/meps09058

    Article  Google Scholar 

  • Quintana F, Wilson R, Dell’Arciprete P, Shepard E, Gómez Laich A (2011) Women from Venus, men from Mars: Inter-sex foraging differences in the imperial cormorant Phalacrocorax atriceps a colonial seabird. Oikos 120:350–358. https://doi.org/10.1111/j.1600-0706.2010.18387.x

    Article  Google Scholar 

  • Quintana F, Wilson R, Prandoni N, Svagelj WS, Gómez-Laich A (2022) Long-term ecology studies in Patagonian seabirds: a review with the imperial cormorant as a case study. In: Helbling EW, Narvarte MA, González RA, Villafañe VE (eds) Global change in Atlantic coastal Patagonian ecosystems. Natural and social sciences of Patagonia. Springer, Cham

    Google Scholar 

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    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. Methods Ecol Evol 4:612–618. https://doi.org/10.1111/2041-210X.12048

    Article  Google Scholar 

  • Tombari AD, Gosztonyi A, Echeverría DD, Volpedo AV (2010) Morfología de los otolitos y las vértebras de especies de aterínidos marinos (Atheriniformes, Atherinopsidae) que coexisten en el Océano Atlántico sudoccidental. Cienc Mar 36:213–223. https://doi.org/10.7773/cm.v36i3.1692

    Article  Google Scholar 

  • Torroglosa ME, Quiroga MV, Cassia MC (2012) Morphometric analysis of sagitta otolith of Salilota australis (Günther, 1878) (Pisces: Moridae) of the southern Patagonian shelf, Argentina. Rev Invest Desarr Pesq 21:81–86

    Google Scholar 

  • Tramer EJ (1969) Bird species diversity: components of Shannon’s formula. Ecology 50:927–929. https://doi.org/10.2307/1933715

    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 

  • Volpedo A, Echeverría D (2000) Catálogo y claves de otolitos para la identificación de peces del Mar Argentino. Dunken, Buenos Aires

    Google Scholar 

  • Votier SC, Bearhop S, Witt MJ et al (2010) Individual responses of seabirds to commercial fisheries revealed using GPS tracking, stable isotopes and vessel monitoring systems. J Appl Ecol 47:487–497. https://doi.org/10.1111/j.1365-2664.2010.01790.x

    Article  Google Scholar 

  • Wunderle JM (1991) Age-specific foraging proficiency in birds. Curr Ornithol 8:273–324

    Google Scholar 

  • Yorio P, Copello S, Kuba L, Gosztonyi A, Quintana F (2010) Diet of imperial cormorants Phalacrocorax atriceps breeding at Central Patagonia, Argentina. Waterbirds 33:70–78. https://doi.org/10.1675/063.033.0108

    Article  Google Scholar 

  • Yorio P, Ibarra C, Marinao C (2017) Induced regurgitation versus stomach sampling: assessing their value for the characterization of imperial cormorant (Phalacrocorax atriceps) diet. Waterbirds 40:162–167. https://doi.org/10.1675/063.040.0208

    Article  Google Scholar 

  • Zhu G, Zhang H, Yang Y, Wang S, Wei L, Yang Q (2018) Upper trophic structure in the Atlantic Patagonian shelf break as inferred from stable isotope analysis. J Oceanol Limnol 36:717–725. https://doi.org/10.1007/s00343-018-6340-5

    Article  Google Scholar 

Download references

Acknowledgements

This research was supported by the Universidad Nacional de la Patagonia Austral (UNPA) and the Wildlife Conservation Society (WCS Argentina). We thank Fundación Temaikén for providing field and laboratory assistants. Special thanks to Evangelina Laztra, Camila MacLaughlin and Edgardo Balverdi for their help in the field and in the laboratory. We would also like to thank the following researchers from CENPAT-CONICET: Nestor García, Atila Gosztonyi and Cyntia Ibarra for their help in the identification of fish otoliths and bones. We thank Nicu-Viorel from the Center for stable isotope, University of New Mexico, for the analysis of pellet membrane. All samples were collected under permission of the competent authority from the Santa Cruz Province. We are also grateful to Carolina Mirallas from the Scientific English Laboratory of the UNPA for improving the language of the manuscript. Finally, we would like to thank two anonymous reviewers for their useful comments that helped improving the manuscript.

Funding

This study was funded by Universidad Nacional de la Patagonia Austral (research projects PI29/B154 & PI29/B199) and by Wildlife Conservation Society (WCS Argentina).

Author information

Authors and Affiliations

  1. Centro de Investigaciones de Puerto Deseado, Universidad Nacional de la Patagonia Austral, Av. Prefectura s/n, 9050, Puerto Deseado, Santa Cruz, Argentina

    Annick Morgenthaler, Ana Millones, Patricia Gandini & Esteban Frere

  2. Centro de Investigaciones y Transferencia (CIT) Golfo San Jorge, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Ruta 1 - Km 4 s/n, Comodoro Rivadavia, Chubut, Argentina

    Annick Morgenthaler

  3. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Av. Prefectura s/n, 9050, Puerto Deseado, Santa Cruz, Argentina

    Patricia Gandini & Esteban Frere

Authors
  1. Annick Morgenthaler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana Millones
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Patricia Gandini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Esteban Frere
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. AMo and AMi conducted field work. AMo and several assistants conducted laboratory analyses of pellets, with the help of AMi. AMo prepared the samples for stable isotope analysis. AMo analysed and interpreted the data under the supervision of AMi, EF and PG. EF and PG obtained the external funding. The first draft of the manuscript was written by AMo with substantial input from EF. All authors contributed to the article revision and final approval.

Corresponding author

Correspondence to Annick Morgenthaler.

Ethics declarations

Conflict of interest

All the authors declared that they have no conflict of interest.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Morgenthaler, A., Millones, A., Gandini, P. et al. Diet of adult and immature imperial cormorants, Leucocarbo atriceps, from southern Patagonia. A combined dietary approach and an exploratory analysis of stable isotopes of pellet membrane. Polar Biol 45, 1529–1539 (2022). https://doi.org/10.1007/s00300-022-03086-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-022-03086-5

Keywords

Search

Navigation