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Journal of Ornithology

, Volume 161, Issue 1, pp 137–147 | Cite as

A multi-isotope and morphometric analysis to uncover ecological niche divergence in two endemic island birds from Madagascar: the Dark and Common Newtonia (Vangidae)

  • Elizabeth Yohannes
  • Friederike WoogEmail author
Original Article

Abstract

The common ancestry of congeneric species implies that their morphology and ecology are similar, and thus that these closely related species may experience intensified levels of competition when sympatrically distributed. Under such circumstances, selective pressure may lead to niche partitioning between and within species, with segregation achieved through variation in morphology, ecology and life history. Examining the mechanisms underlying the coexistence or segregation of congeneric species requires detailed data on aspects of their ecology such as their feeding behaviour or habitat use. Endemic island birds, such as the vangas of Madagascar, are good candidates for studying processes of niche segregation. Vangas underwent rapid speciation following the initial colonization of the island by a shared ancestor and now provide a prime example of adaptive radiation, with considerable variation in body size and shape. Four small species of Newtonia are an exception to this variation, as they show morphological overlap and partial spatial range sympatry. Here, we describe the morphology of two Newtonia species, the Common Newtonia Newtonia brunneicauda and Dark Newtonia Newtonia amphichroa, with respect to their ecology and trophic niches using a multi-isotope approach (stable isotope ratios of carbon, nitrogen and sulphur). We report evidence for adaptations involving morphological feeding traits and provide data on contrasting trophic niches between two species with a close phylogenetic relationship. We document micro-habitat niche specialization that may be due to vertical stratification within the forest. Differences in feather isotopic signatures indicate different nutrient sources and point towards microhabitat segregation that is sufficient to maintain species integrity and permit coexistence.

Keywords

Stable carbon isotope ratio Stable nitrogen isotope ratio Stable sulphur isotope ratio Adaptation Morphology Vangidae 

Zusammenfassung

Ökologische Einnischung zweier endemischer Vogelarten in Madagaskar: Stabile Isotope und Morphometrie bei Rostbauch- und Olivbauchnewtonien (Vangidae)

Nahe verwandte Arten der gleichen Gattung sind einander in Morphologie und Ökologie oft ähnlich. Kommen sie im gleichen Gebiet vor, sollten sie sich in ihrer ökologischen Nische unterscheiden, um eine erhöhte Konkurrenz zu vermeiden. Selektive Kräfte wirken auf Variationen in Morphologie, Ökologie, Verhalten und anderen Lebensparametern innerhalb und zwischen Arten. Um die Koexistenz oder Auftrennung von nahe verwandten und sympatrisch vorkommenden Taxa zu untersuchen, sind genaue Daten zur Ökologie wie z.B. der Nahrungsökologie oder der Habitatnutzung notwendig. Endemische Inselvögel wie die Vangawürger (Vangidae) Madagaskars sind gut zur Untersuchung der Nischenaufspaltung geeignet. Nach der Erstbesiedlung Madagaskars zeigten die Vangawürger eine rasche Artbildung aus einem gemeinsamen Vorfahr und sind heute ein Paradebeispiel für adaptive Radiation. Sie zeigen eine große Variation in Körpergröße, Gestalt und Schnabelform. Vier kleine Arten der Gattung Newtonia stellen eine Ausnahme dar, da sie sich morphologisch überlappen und in Teilen ihres Verbreitungsgebiets sympatrisch vorkommen. Newtonien sind vor allem im Regenwald oft nur schwer zu beobachten, daher wurden die Tiere für die Studie in Japannetzen gefangen und nach dem Messen und Beproben wieder frei gelassen. Wir untersuchten die Morphologie von zwei Arten, die sympatrisch im Maromizaha-Regenwald im Osten Madagaskars vorkommen: der Rostbauch- (Newtonia brunneicauda) und der Olivbauchnewtonie (Newtonia amphichroa). Deren trophische Nische beschreiben wir mittels der Zusammensetzung stabiler Isotope in den Federn (Kohlenstoff δ13C, Stickstoff δ15N und Schwefel δ34S). Obwohl äußerlich zunächst ähnlich, unterschieden sich die zwei Arten in ihrer Morphologie: Olivbauchnewtonien hatten stärkere Schnäbel und längere Tarsen als Rostbauchnewtonien, was darauf hindeutet, dass sie auf etwas größere Beute spezialisiert sind und stärkere Zweige nutzen. Während beide Arten ähnliche δ15N- und δ34S-Werte aufwiesen, zeigten Olivbauchnewtonien geringere Werte beim δ13C. In anderen Studien zeigten Tiere, die im Wald weiter unten vorkommen, niedrigere Werte von δ13C, was gut mit unseren Ergebnissen zusammenpasst, zudem wir die Olivbauchnewtonien im Schnitt in geringeren Netzhöhen als Rostbauchnewtonien gefangen hatten. Beide Newtonienarten scheinen sowohl durch ihre unterschiedliche Morphologie und der daraus resultierenden Unterschiede in der Art der Nahrungssuche und -aufnahme sowie durch die Unterschiede in ihrer vertikalen Habitatnutzung ausreichend getrennt, um sich im gleichen Gebiet keine Konkurrenz zu machen.

Notes

Acknowledgements

We are indebted to the Malagasy authorities for granting all the relevant research and export permits and to the Groupe d’Étude et de Recherche sur les Primates de Madagascar, namely Jonah Ratsimbazafy and Rose Marie Randrianarison, for letting us work at Maromizaha. This work would not have been possible without the continued support over many years of Haja Rakotomanana and Daniel Rakotondravony at the Department of Animal Biology, University of Antananarivo. We thank Jean-Robert Lekamisi, Lova Rasolondraibe Lovahasina Tahiry, Nicola Lillich, Pia Reufsteck and all the other Malagasy and German assistants for their help in the field. We thank Wolfgang Kornberger and Claudia Greis for their assistance in the laboratory and Amy-Jane Beer (www.wildstory.co.uk) for the language editing. The research conducted complies with the current laws of the country in which it was performed.

Compliance with ethical standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and animal rights

No animals were harmed during the study.

References

  1. Araújo M, Guisan A (2006) Five (or so) challenges for species distribution modeling. J Biogeogr 33:1677–1688Google Scholar
  2. Bearhop S, Adams CE, Waldron S, Fuller RA, MacLeod H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012Google Scholar
  3. Bonafini M, Pellegrini M, Ditchfield P, Pollard AM (2013) Investigation of the ‘canopy effect’ in the isotope ecology of temperate woodlands. J Archaeol Sci 40:3926–3935Google Scholar
  4. Brandl R, Kristin A, Leisler B (1994) Dietary niche breadth in a local community of passerine birds: an analysis using phylogenetic contrasts. Oecologia 98:109–116PubMedGoogle Scholar
  5. Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125Google Scholar
  6. Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago Press, ChicagoGoogle Scholar
  7. Chesson P (2000) General theory of competitive coexistence in spatially-varying environments. Theor Popul Biol 58:211–237PubMedGoogle Scholar
  8. Dawideit BA, Phillimore AB, Laube I, Leisler B, Böhning-Gaese K (2009) Ecomorphological predictors of natal dispersal distances in birds. J Anim Ecol 78:388–395PubMedGoogle Scholar
  9. Drucker DG, Bridault A, Hobson KA, Szuma E, Bocherens H (2008) Can carbon δ13C in large herbivores reflect the canopy effect in temperate and boreal ecosystems? Evidence from modern and ancient ungulates. Palaeogeogr Palaeoclimatol Palaeoecol 266:69–82Google Scholar
  10. Eck S, Fiebig J, Heynen I, Fiedler W, Nicolai B, Töpfer T, Van den Elzen R, Winkler R, Woog F (2011) Measuring birds. Deutsche Ornithologen, RadolfzellGoogle Scholar
  11. Eguchi K, Yamagishi S, Randrianasolo V (1993) The composition and foraging behaviour of mixed species flocks of forest living birds in Madagascar. Ibis 135:91–96Google Scholar
  12. Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Austral J Plant Physiol 9:121–137Google Scholar
  13. Forstmeier W, Bourski OV, Leisler B (2001) Habitat choice in Phylloscopus warblers: the role of morphology, phylogeny and competition. Oecologia 128:566–576PubMedGoogle Scholar
  14. Goodman SM, Parrillo P (1997) A study of the diets of Malagasy birds based on stomach contents. Ostrich 68:104–113Google Scholar
  15. Goodman SM, Pidgeon M, Hawkins AFA, Schulenberg TS (1997) The birds of south-eastern Madagascar. Field Zool 87:1–132Google Scholar
  16. Grant PR, Price TD (1981) Population variation in continuously varying traits as an ecological genetics problem. Am Zool 21:795–811Google Scholar
  17. Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326PubMedGoogle Scholar
  18. Holt RD (1984) Spatial heterogeneity, indirect interactions, and the coexistence of prey species. Am Nat 124:377–406PubMedGoogle Scholar
  19. Holt RA, Lawton JH (1994) The ecological consequences of shared natural enemies. Annu Rev Ecol Syst 25:495–520Google Scholar
  20. Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER−Stable stable isotope Bayesian ellipses in R. J Anim Ecol 80:595–602PubMedGoogle Scholar
  21. Jønsson KA, Fabre PH, Fritz SA, Etienne RS, Ricklefs RE, Jørgensen TB, Fjeldså J, Rahbek C, Ericson GP, Woog F, Pasquet E, Irestedt M (2012) Ecological and evolutionary determinants for the adaptive radiation of the Madagascan vangas. Proc Natl Acad Sci 109:6620–6625PubMedGoogle Scholar
  22. Kipp FA (1959) Der Handflügel-Index als flugbiologisches Maß. Vogelwarte 20:77–86Google Scholar
  23. Kohn MJ (2010) Carbon isotope compositions of terrestrial C3 plants as indicators of (paleo) ecology and (paleo) climate. Proc Natl Acad Sci 107:19691–19695PubMedGoogle Scholar
  24. Krouse HR, Stewart JWB, Grinenko VA (1991) Pedosphere and biosphere. In: Krouse HR, Grinenko VA (eds) Stable isotopes: natural and anthropogenic sulphur in the environment. Wiley, Toronto, pp 267–306Google Scholar
  25. Langrand O (1990) Guide to the birds of Madagascar. Yale University Press, New HavenGoogle Scholar
  26. Layman CA, Quattrochi JP, Peyer CM, Allgeier JE (2007) Niche width collapse in a resilient top predator following ecosystem fragmentation. Ecol Lett 10:937–944PubMedPubMedCentralGoogle Scholar
  27. Leisler B, Ley HW, Winkler H (1989) Habitat, behaviour and morphology of Acrocephalus warblers: an integrated analysis. Ornis Scand 20:181–186Google Scholar
  28. Lewis S, Schreiber EA, Daunt F, Schenk AG, Orr K, Adams A, Wanless S, Hamer CK (2005) Sex-specific foraging behaviour in tropical boobies: does size matter? Ibis 147:408–414Google Scholar
  29. Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11:995–1003PubMedGoogle Scholar
  30. Losos JB, Ricklefs RE (2009) Adaptation and diversification on islands. Nature 457:830PubMedGoogle Scholar
  31. May RM, Mac Arthur RH (1972) Niche overlap as a function of environmental variability. Proc Natl Acad Sci 69:1109–1113PubMedGoogle Scholar
  32. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140Google Scholar
  33. Moll JD, Brown JS (2008) Competition and coexistence with multiple life history stages. Am Nat 171:839–843PubMedGoogle Scholar
  34. Morris P, Hawkins F (1998) Birds of Madagascar: a photographic guide. Yale University Press, New HavenGoogle Scholar
  35. Parnell A, Jackson A (2013) SIAR: stable isotope analysis in R. R package version 4.2. http://CRAN. R-projectGoogle Scholar
  36. Pocheville A (2015) The ecological niche: history and recent controversies. In: Heams T, Huneman P, Lecointre G, Silberstein M (eds) Handbook of evolutionary thinking in the sciences. Springer, Dordrecht, pp 547–586Google Scholar
  37. Pulliam HR (2000) On the relationship between niche and distribution. Ecol Lett 3:349–361Google Scholar
  38. Rand AL (1936) The distribution and habits of Madagascar birds: summary of the field notes of the Mission Zoologique Franco-Anglo-Americaine à Madagascar. American Museum of Natural History, New YorkGoogle Scholar
  39. Reddy S, Driskell A, Rabosky D, Hackett S, Schulenberg T (2012) Diversification and the adaptive radiation of the vangas of Madagascar. Proc R Soc B 279:2011–2380Google Scholar
  40. Redfern CPF, Clark JA (2001) Ringers’ manual. British Trust for OrnithologyGoogle Scholar
  41. Reuter KE, Wills AR, Lee RW, Cordes EE, Sewall BJ (2016) Using stable isotopes to infer the impacts of habitat change on the diets and vertical stratification of frugivorous bats in Madagascar. PLOS ONE 11:e0153192PubMedPubMedCentralGoogle Scholar
  42. Rex K, Michener R, Kunz TH, Voigt CC (2011) Vertical stratification of Neotropical Leaf-nosed Bats (Chiroptera: Phyllostomidae) revealed by stable carbon isotopes. J Trop Ecol 27:211–222Google Scholar
  43. Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352Google Scholar
  44. Safford R, Hawkins F (2013) The birds of Africa: Volume VIII: The Malagasy region: Madagascar, Seychelles, Comoros, Mascarenes, vol 8. Black, LondonGoogle Scholar
  45. Sall J, Lehman A, Stephens ML, Creighton L (2012) Start statistics: a guide to statistics and data analysis using JMP. SAS InstituteGoogle Scholar
  46. Schulenberg TS (2003) The radiation of passerine birds on Madagascar. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 1130–1134Google Scholar
  47. Taper ML, Case TJ (1985) Quantitative genetic models for the coevolution of character displacement. Ecology 66:355–371Google Scholar
  48. van der Merwe NJ, Medina E (1991) The canopy effect, carbon isotope ratios and food-webs in Amazonia. J Archaeol Sci 18:249–259Google Scholar
  49. Vogel JC (1978) Recycling of CO2 in a forest environment. Oecol Plant 13:89–94Google Scholar
  50. Winkler H, Leisler B (1992) On the ecomorphology of migrants. Ibis 134:21–28Google Scholar
  51. Woog F, Ramanitra N (2008) Site fidelity of some rainforest species endemic to Madagascar. J Ornithol 147(5 Suppl. 1):275Google Scholar
  52. Woog F, Ramanitra N, Rasamison S (2006) Effects of deforestation on eastern Malagasy bird communities. In: Schwitzer C, Brandt S, Ramilijaona O, Rakotomalala Razanahoera M, Ackermand D, Razakamanana T, Ganzhorn J (eds) Proceedings of the German-Malagasy research cooperation in life and earth sciences: concept. Verlag, Berlin, pp 203–214Google Scholar
  53. Woog F, Ramanitra N, Rasamison SA, Tahiry RL (2018) Longevity in some Malagasy rainforest passerines. Ostrich 89:281–286Google Scholar
  54. Yamagishi S, Eguchi K (1996) Comparative foraging ecology of Madagascar vangids (Vangidae). Ibis 138:283–290Google Scholar
  55. Yamagishi S, Honda M, Eguchi K, Thorstrom R (2001) Extreme endemic radiation of the Malagasy vangas (Aves: Passeriformes). J Mol Evol 53:39–46PubMedGoogle Scholar

Copyright information

© Deutsche Ornithologen-Gesellschaft e.V. 2019

Authors and Affiliations

  1. 1.Institute for Limnology, Stable Isotope LabUniversity of KonstanzKonstanzGermany
  2. 2.Staatliches Museum für Naturkunde StuttgartStuttgartGermany

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