Cookies Policy

This site uses cookies. By continuing to browse the site you are agreeing to our use of cookies.

I accept this policy

Find out more here

Diversity metrics, species turnovers and nestedness of bird assemblages in a deep karst sinkhole

No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.
The full text of this article is not currently available.

Brill’s MyBook program is exclusively available on BrillOnline Books and Journals. Students and scholars affiliated with an institution that has purchased a Brill E-Book on the BrillOnline platform automatically have access to the MyBook option for the title(s) acquired by the Library. Brill MyBook is a print-on-demand paperback copy which is sold at a favorably uniform low price.

Access this article

+ Tax (if applicable)
Add to Favorites
You must be logged in to use this functionality

image of Israel Journal of Ecology and Evolution

We reported a study on breeding birds occurring inside an 80 m-deep karst sinkhole, with the characterization of the assemblages recorded along its semi-vertical slopes from the upper edge until the bottom. The internal sides of the sinkhole have been vertically subdivided in four belts about 20 m high. The highest belt (at the upper edge of the cenote) showed the highest values in mean number of bird detections, mean and normalized species richness, and Shannon diversity index. The averaged values of number of detections and species richness significantly differ among belts. Species turnover (Cody’s β-diversity) was maximum between the highest belts. Whittaker plots showed a marked difference among assemblages shaping from broken-stick model to geometric series, and explicited a spatial progressive stress with a disruption in evenness towards the deepest belts. Bird assemblages evidenced a nested subset structure with deeper belts containing successive subsets of the species occurring in the upper belts. We hypothesize that, at least during the daytime in breeding season, the observed non-random distribution of species along the vertical stratification is likely due to (i) the progressive simplification both of the floristic composition and vegetation structure, and (ii) the paucity of sunlight as resources from the upper edge to the inner side of the cenote.

Affiliations: 1: “Torre Flavia” LTER (Long Term Ecological Research) Station, Città Metropolitana di Roma Capitale, Servizio Aree Protette, Via Tiburtina 691, 00159 Roma, Italia and Dipartimento di Scienze, Università degli Studi di Roma Tre, Viale Marconi 446, 00146 Rome. E-mail:; ; 2: Servizio Aree protette, Città Metropolitana di Roma Capitale, via Tiburtina, 691, 00159 Rome, Italy; ; 3: Dipartimento di Biologia Ambientale, Università di Roma ‘Sapienza’, Piazzale Aldo Moro, 5, 00185 Rome, Italy. E-mail:; ; 4: Sustainable Development Foundation, via Garigliano 61/a, 00198 Rome, Italy. E-mail:; ; 5: Dipartimento di Scienze, Università degli Studi di Roma Tre, Viale Marconi 446, 00146 Rome, Italy. E-mail:


Full text loading...


Data & Media loading...

1. Acevedo MA,, Mitchell Aide T. 2008. "Bird community dynamics and habitat associations in Karst", Mangrove and Pterocarpus forest fragments in an urban zone in Puerto Rico. Caribb J Sc.Vol 44:402416.
2. Almeida-Neto M,, Guimaraes P,, Guimaraes PR,, Lodola RD,, Ulrich W. 2008. "A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement". OikosVol 117:12271239. [Crossref]
3. Angulo B,, Morales T,, Uriarte JA,, Antiguedad I. 2013. "Implementing a comprehensive approach for evaluating significance and disturbance in protected karst areas to guide management strategies". J Environm Manag.Vol 130:386396. [Crossref]
4. Barr TC,, Holsinger JR. 1985. "Speciation in Cave Faunas". Ann Rev Ecol System.Vol 16:313337. [Crossref]
5. Bátori Z,, Gallé R,, Erdõs L,, Körmöczi L. 2011. "Ecological conditions, flora and vegetation of a large doline in the Mecsek Mountains (South Hungary)". Acta Bot Croat.Vol 70:147155.
6. Bátori Z,, Csiky J,, Farkas T,, Vojtkó AE,, Erdõs L,, Kovacs D,, Wirth T,, Kormoczi L,, Tölgyesi C,, Körmöczi L,, Vojtkó A. 2014. "A comparison of the vegetation of forested and non-forested solution dolines in Hungary: a preliminary study". Intern J Speleol.Vol 43:1526. [Crossref]
7. Battisti C,, Dodaro G,, Franco D. 2014. "The data reliability in ecological research: a proposal for a quick self-assessment tool". Natur Hist Sc.Vol 1:7579. [Crossref]
8. Battisti C,, Poeta G,, Fanelli G. 2016. An introduction to Disturbance Ecology. A road map for wildlife management and conservation. Springer, The Netherland.
9. Bellamy PE,, Hinsley SA,, Newton I. 1996. "Factors influencing bird species numbers in small woods in south-east England". J Appl Ecol.Vol 33:249262. [Crossref]
10. Bianconi R,, Battisti C,, Zapparoli M. 2004. "Pattern of richness, abundance and diversity of four interior bird species in a hilly landscape in Central Italy: a contribution to assess their sensitivity to habitat fragmentation". J Medit Ecol.Vol 3–4:3744.
11. Bibby CJ,, Burgess ND. 1992. Bird census techniques. London: Academic Press.
12. Bono P. 2001. "Is the “Merro Well” the deepest karst cenote explored in the world?" Environm Geol. Vol 40:787788.
13. Brichetti P,, Fracasso G. 2015. "Check-list degli uccelli italiani aggiornata al 2014". Riv Ital Ornit. Vol 85:3150.
14. Camprodon J,, Brotons L. 2006. "Effects of undergrowth clearing on the bird communities of the Northwestern Mediterranean Coppice Holm oak forests". Forest Ecol Manag.Vol 221:7282. [Crossref]
15. Cieslak M. 1985. "Influence of forest size and other factors on breeding bird species number". Ekol Polska.Vol 33:103121.
16. Cody ML,. 1975. "Towards a theory of continental species diversity: bird distribution Mediterranean habitat gradients". In: Cody ML,, Diamond JM, editors. Ecology and evolution of communities. Cambridge, Harvard University Press, pp. 214257.
17. Cokendolpher JC,, Polyak VJ. 1996. "Biology of the Caves at Sinkhole Flat, Eddy County, New Mexico". J Cave Karst St.Vol 58:181192.
18. Culver DC. 2016. "Karst environment". Zeitschrift Geomorphol.Vol 60:103117. [Crossref]
19. Culver DC,, Master LL,, Christmas MC,, Hobbs HH. 2000. "Obligate cave fauna of the 48 contiguous United States". Conserv Biol.Vol 14:386401. [Crossref]
20. Dabelsteen T,, Larsen ON,, Podorson SBJ. 1993. "Habitat-induced degradation of sound signals: Quantifying the effects of communication sounds and bird location on blur ratio, excess attenuation, and signal-to-noise ratio in black bird song". Acoust Soc Amer J.Vol 93:22062220. [Crossref]
21. Day M,, Urich P. 2000. "An assessment of protected karst landscapes in Southeast Asia". Cave Karst Sc.Vol 27:6170.
22. Dornelas M,, Soykan CU,, Ugland KI,. 2011. "Biodiversity and disturbance". In: Magurran A,, McGill BJ, editors, Biological diversity. Frontiers in measurements and assessments. Oxford: University Press, Oxford, pp. 237251.
23. Dytham C. 2011. Choosing and using statistics: a biologist’s guide. London: John Wiley and Sons.
24. Fracasso G,, Baccetti N,, Serra L. 2009. "La lista CISO-COI degli Uccelli italiani". Parte prima: liste A, B e C. Avocetta.Vol 33:524.
25. Freckleton RP,, Watkinson AR,, Green RE,, Sutherland WJ. 2006. "Census error and the detection of density dependence". J Anim Ecol.Vol 75:837851. [Crossref]
26. Friend S. 2002. Sinkholes. Pineapple Press Inc.
27. Gary MO,, Sharp JM Jr,, Caramanna G,, Havens RH. 2003. Volcanically influenced speleogenesis: forming El Sistema Zacatòn, Mexico, and Pozzo del Merro, Italy, the deepest phreatic sinkholes in the world: Geological Society of America Abstracts with Programs 34, session 19–4:152.
28. Gerrard SP. 2015. The Cenotes of the Riviera Maya. Page Publishing Inc.
29. Giardini M., 2012a. "Il Pozzo del Merro: aspetti botanici". In: Giardini M, editor, Sant’Angelo Romano (Monti Cornicolani, Roma). Un territorio ricco di storia e di natura. Comune di Sant’Angelo Romano, Regione Lazio – Assessorato Ambiente e Sviluppo sostenibile, Grafica Ripoli, Tivoli, pp. 286293.
30. Giardini M. (ed.). 2012b. "Sant’Angelo Romano (Monti Cornicolani, Roma)". Un territorio ricco di storia e di natura. Comune di Sant’Angelo Romano, Regione Lazio – Assessorato Ambiente e Sviluppo sostenibile, Grafica Ripoli, Tivoli.
31. Giardini M,, Caramanna G,. 2012. "Il Pozzo del Merro: storia delle ricerche e situazione attuale". In: Gardini M, editor, Sant’Angelo Romano (Monti Cornicolani, Roma). Un territorio ricco di storia e di natura, Comune di Sant’Angelo Romano, Regione Lazio – Assessorato Ambiente e Sviluppo sostenibile, Grafica Ripoli, Tivoli, pp. 265273.
32. Giardini M,, Caramanna G,, Calamita U. 2001. "L’imponente sinkhole del Pozzo del Merro (Monti Cornicolani, Roma): stato attuale delle conoscenze". Natura e Montagna.Vol 48:1227.
33. Guthery FS. 2007. "Deductive and inductive methods of accumulating reliable knowledge in wildlife science". J Wild Manag. Vol 71:222225.
34. Hamilton-Smith E. 2001. "Current initiatives in the protection of karst biodiversity". Natura Croat.Vol 10:229242.
35. Hermansen JS,, Sæther SA,, Elgvin TO,, Borge T,, Hjelle E,, Sætre G-P. 2011. "Hybrid speciation in sparrows I: phenotypic intermediacy, genetic admixture and barriers to gene flow". Molec Ecol.Vol 20:38123822. [Crossref]
36. Hicks LE. 1938. "A Unique Population of Water Birds in Northern Ohio: 1937". Wilson Bull.Vol 50:197200.
37. Hinsley SA,, Bellamy PE,, Newton I,, Sparks TH. 1995. "Habitat and landscape factors influencing the presence of individual breeding bird species in woodland fragments". J Avian Biol.Vol 26:94104. [Crossref]
38. Hutchinson JMC. 1999. "Factors influencing the surface fauna of inland blue holes on South Andros", Bahamas. Bahamas J Sc.Vol 6:2943.
39. Keiller BM. 2011. The impact of sinkholes on species richness and diversity: implications for mine rehabilitation. Doctoral dissertation. Available on:
40. Klaas EE. 2011. Summer Birds from the Yucatan Peninsula. Project Gutenberg.
41. Koleff P,, Gaston KJ,, Lennon JJ. 2003. Measuring beta diversity for presence–absence data. J Anim Ecol.Vol 72:367382. [Crossref]
42. Kroodsma DE,, Byers BE. 1991. "The function(s) of bird song". Am Zool.Vol 31:318328. [Crossref]
43. Iannilli V,, Vigna Taglianti A. 2005. "New data of the genus Niphargus (Amphipoda, Niphargidae) in Italy, with description of a new species of the orcinus group". CrustaceanaVol 77:12531261.
44. James FC,, Shugart HH. 1970. "A quantitative method of habitat description". Audubon Field Not.Vol 24:727736.
45. Jones WK,, Hobbs III HH,, Wicks CM,, Currle RR,, Hose LD,, Kerbo RC,, Goodbar JR,, Trout J. 2003. "Recommendations and guidelines for managing caves on protected lands". Karst Waters Institute, special publication 8. Charles Town.
46. Lewin J,, Woodward JC,. 2007. "Karst geomorphology and environmental change". In: Woodward J, editor, The Physical Geography of the Mediterranean. Oxford: Oxford University Press, pp. 287317.
47. Li C,, Xiong K,, Wu G. 2013a. "Process of biodiversity research of Karst areas in China". Acta Ecol Sinica.Vol 33:192200. [Crossref]
48. Li Z,, Lu Z,, Shu X,, Jiang G,, Xu L,, Zhou F. 2013b. "Nestedness of bird assemblages in the karst forest fragments of southwestern Guangxi, China". Chinese BirdsVol 4:170183. [Crossref]
49. Lloyd M,, Ghelardi RJ. 1964. "A table for calculating the equitability component of species diversity". J Anim Ecol.Vol 33:217225. [Crossref]
50. Lorenzetti E,, Battisti C. 2007. "Nature reserve selection on forest fragments in a suburban landscape (Rome, Central Italy): indications from a set of avian species". Landsc Res. Vol 32:5778. [Crossref]
51. Magurran A. 2004. Measuring Biological Diversity. London: Blackwell.
52. Magurran A,, McGill BJ. 2011. Biological diversity. Frontiers in measurements and assessments. Oxford, Oxford University Press.
53. Møller AP. 1987. "Breeding birds in habitat patches: random distribution of species and individuals?" J BiogeogrVol 14:225236. [Crossref]
54. Opdam P,, Rijsdijk G,, Hustings F. 1985. "Bird communities in small woods in an agricultural landscape: effects of area and isolation". Biol Conserv.Vol 34:333352. [Crossref]
55. Orłowski G,, Martini K,, Martini M. 2008. "Avian responses to undergrowth removal in a suburban wood". Polish J Ecol.Vol 56:487495.
56. Özkan K,, Gulsoy S,, Mert A,, Ozturk M,, Muys B. 2010. "Plant distribution-altitude and landform relationships in karstic sinkholes of Mediterranean region of Turkey". J Environm Biol.Vol 31:5160.
57. Palozzi R,, Caramanna G,, Albertano P,, Congestri R,, Bruno L,, Romano R,, Giganti MG,, Zenobi R,, Costanzo C,, Valente G,, Polani D,, Vecchio M,, Vinci M,, Sbordoni V. 2010. "The underwater exploration of the Merro sinkhole and the associated diving physiological and psychological effects". Underwater Techn. Vol 29:125134.
58. Polli E. 2005. "Aspetti speleo-vegetazionali della “Jama Dimnice”, 736 S (“Grotta del Fumo”, 626 VG) nel Matarsko Podolje (Valsecca di Castelnuovo) di Markošc�ina (Carso sloveno). Contributo alla conoscenza della speleoflora vascolare carsica". Atti Mem Comm Grotte “E. Boegan”.Vol 40:6383.
59. Reynolds JD. 2014. "Preliminary notes on three turloughs (temporary ponds overlying karst) in County Limerick, with comments on their vegetation and water beetle fauna". Biology and Environment, Proceed Royal Irish Acad. 114.
60. Rimmer CC,, Townsend JM,, Townsend AK,, Fernández EM,, Almonte J. 2005. "Avian Diversity, Abundance, And Conservation Status" In The Macaya Biosphere Reserve of Haiti. Ornitol Neotrop.Vol 16:219230.
61. Roble SM,, Stevenson DJ. 1998. "Records of Odonata, Fish, and Birds from the Grafton Ponds Sinkhole Complex, York County", Virginia. Banisteria.Vol 12:317.
62. Romano A,, Salvidio S,, Palozzi R,, Sbordoni V. 2012. "Diet of the newt, Triturus carnifex (Laurenti, 1768), in the flooded karst sinkhole Pozzo del Merro, central Italy". J Cave Karst St.Vol 74:271277. [Crossref]
63. Romesburg HC. 1981. "Wildlife science: gaining reliable knowledge". J Wildl Manag. Vol 45:293313.
64. Rodriguéz-Gironés MA,, Santamarìa L. 2006. "A new algorithm to calculate the nestedness temperature of presence-absence matrices". J Biogeogr.Vol 33:924935. [Crossref]
65. Sauro U. 1993. "Human impact on the karst of the Venetian Fore-Alps", Italy. Environm Geol.Vol 21:115121. [Crossref]
66. Schmitter-Soto JJ,, Comìn FA,, Escobar-Briones E,, Herrera-Silveira J,, Alcocer J,, Suarez- Morales E,, Elìas-Gutierrez M,, Dìaz-Arce V,, Marìn LE,, Steinich B. 2002. "Hydrogeochemical and biological characteristics of cenotes in the Yucatan Peninsula (SE Mexico)". Hydrobiologia.Vol 467:215228. [Crossref]
67. Shannon CE,, Weaver W. 1963. Mathematical theory of communication. Urbana, Illinois: University of Illinois Press.
68. Sorjonen J. 1986. "Factors affecting the structure of song and the singing behaviour of some northern European passerine birds". Behaviour.Vol 98:286304. [Crossref]
69. SPSS Inc. 2003. SPSS for Windows – Release 13.0 (1 Sep 2004), Leadtools (c), Lead Technologies Inc.
70. Strona G,, Nappo D,, Boccacci F,, Fattorini S,, San-Miguel-Ayanz J. 2014. "A fast and unbiased procedure to randomize ecological binary matrices with fixed rows and column totals". Nature comm.Vol 5:4114.
71. Sutherland W. 2006. Ecological Census Techniques. Cambridge: Cambridge University Press.
72. Tews J,, Brose U,, Grimm V,, Tielbörger K,, Wichmann MC,, Schwager M,, Jeltsch F. 2004. "Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures". J Biogeogr.Vol 31:7992. [Crossref]
73. Tomiaojæ L,, Bursell J. 2006. "Why dark plumage of the European Blackbirds Turdus merula?" Lundiana.Vol 7:127132.
74. Toms JD,, Schmiegelow FK,, Hannon SJ,, Villard M-A. 2006. "Are point counts of boreal songbirds reliable proxies for more intensive abundance estimators?" Auk.Vol 123:438454. [Crossref]
75. Ulrich W,, Gotelli NJ. 2007. "Null model analysis of species nestedness patterns". Ecology.Vol 88:18241831. [Crossref]
76. Urich PB,, Day M,, Lynagh F. 2001. "Policy and practice in karst landscape protection: Bohol, the Philippines". Geograph J.Vol 67:305323.
77. Van Beynen P,, Townsend K. 2005. "A disturbance index for karst environments". Environm Manag. Vol 36:101116.
78. Vilisics F,, Sòlymos P,, Nagy A,, Farkas R,, Kemencei Z,, Hornung E. 2011. "Small scale gradient effects on isopods (Crustacea: Oniscidea) in karstic sinkhole". Biologia.Vol 66:499505.
79. Vrbek M,, Fiedler S. 2000. "The ecological and floristic characteristics of Ledena jama pit on Velebit mountain", Croatia. Natura Croat.Vol 9:115131.
80. Watson J,, Hamilton-Smith E,, Gillieson D,, Kiernan K. 1997. Guidelines for Cave and Karst protection. IUCN, Gland, Switzerland.
81. Whittaker RH. 1965. "Dominance and diversity in land plant communities". Science.Vol 147:250260. [Crossref]
82. Whittow J. 1984. Dictionary of Physical Geography. London: Penguin.
83. Wiens JA. 1989. The Ecology of Bird Communities, Vols. 1 and 2. Cambridge Studies in Ecology, Cambridge: Cambridge University Press.
84. Zangari L,, Ferraguti M,, Battisti C,, Luiselli L,, Bologna MA. 2013. "Breeding birds along a vegetation gradient in a Mediterranean landscape: contrasting patterns in spatial diversity". Vie Milieu.Vol 63:121126.

Article metrics loading...



Can't access your account?
  • Tools

  • Add to Favorites
  • Printable version
  • Email this page
  • Subscribe to ToC alert
  • Get permissions
  • Recommend to your library

    You must fill out fields marked with: *

    Librarian details
    Your details
    Why are you recommending this title?
    Select reason:
    Israel Journal of Ecology and Evolution — Recommend this title to your library
  • Export citations
  • Key

  • Full access
  • Open Access
  • Partial/No accessInformation