Ecological preferences of the endemic reptile community of Socotra

Abstract

The Socotra Archipelago is a unique hotspot of biodiversity, particularly for terrestrial reptiles (28 endemic out of 31 native species) whose ecology is known only in general terms. We describe the ecological preference and the daily activity of 21 species of terrestrial reptiles, geckos, lizards, skinks, snakes and chameleon, from the largest island of the archipelago. The database includes 6950 records collected by 260 standardized transects from 2007 to 2013. The sister species Haemodracon riebeckiiH. trachyrhinus with very distinct body sizes, overlapped in their distribution but segregated by habitat and substrate. Three pairs of sister species with great phylogenetic affinity and similar morphology (Pristurus insignisP. insignoides; Pristurus guichardiP. obsti; Hemidactylus dracaenacolusH. granti) were only partially segregated by distribution, habitat, substrate and body size, in the order of decreasing frequency. On the contrary, the other, phylogenetically more distant species of geckos, widely distributed and less similar in morphology, overlapped completely in their habitat use and distributional range. Such patterns suggest that strictly related species reduced their competition by segregation in different habitats and temporal niches and by non-overlapping distribution within the relatively small island of Socotra. On the other hand, the activity rhythm was similar within each genus. The unique biodiversity of Socotra endured up to present, thanks to a human impact lower than for most other inhabited islands, but the pace of change has accelerated recently. Conservation measures are urgent, particularly for the species of endemic geckos with a distribution range as small as 10 km2.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

(a, c, d, e, f, g photo E. Razzetti; b, h photo R. Sindaco)

References

  1. Agnarsson I, Kuntner M (2012) The generation of a biodiversity hotspot: biogeography and phylogeography of the western Indian Ocean islands. Current topics in phylogenetics and phylogeography of terrestrial and aquatic systems. IntechOpencom. https://doi.org/10.5772/38958

    Article  Google Scholar 

  2. Arnold EN (1986) New species of semaphore gecko (Pristurus: Gekkonidae) from Arabia and Socotra. Fauna Saudi Arabia 8:352–377

    Google Scholar 

  3. Autin J, Bellahsen N, Leroy S, Husson L, Beslier MO, d'Acremont E (2013) The role of structural inheritance in oblique rifting: insights from analogue models and application to the Gulf of Aden. Tectonophysics 607:51–64

    Google Scholar 

  4. Badiane A, Garcia-Porta J, Červenka J, Kratochvíl L, Sindaco R, Robinson MD, Morales H, Mazuc T, Price T, Amat F, Shobrak MY, Wilms T, Simó-Riudalbas M, Ahmadzadeh F, Papenfuss TJ, Cluchier A, Viglione J, Carranza S (2014) Phylogenetic relationships of Semaphore geckos (Squamata: Sphaerodactylidae: Pristurus) with an assessment of the taxonomy of Pristurus rupestris. Zootaxa 3835:33–58

    Google Scholar 

  5. Benda P, Nasher AK, Van Damme K, Vallo P, Reiter A (2017) Bats (Mammalia: Chiroptera) of the Eastern Mediterranean and Middle East. Part 14. Bat fauna of the Socotra Archipelago. Yemen Acta Soc Zool Bohem 81:99–169

    Google Scholar 

  6. Bezděk J, Hájek J (2017) Insect biodiversity of the Socotra Archipelago-underlined and counted. Acta Entomologica Musei Nationalis Pragae 57(s1):1–39

    Google Scholar 

  7. Bosworth W, Huchon P, McClay K (2005) The Red Sea and Gulf of Aden Basins. J Afr Earth Sci 43:334–378

    Google Scholar 

  8. Bütikofer L, Sacchi R, Pupin F, Pellitteri-Rosa D, Razzetti E, Pella F, Fasola M (2013) Sexual dimorphism and allometry of the lacertid Mesalina balfouri (Blanford, 1881), endemic to the Archipelago of Socotra (Yemen) (Squamata: Sauria: Lacertidae). Herpetozoa 25:101–108

    Google Scholar 

  9. Carranza S, Arnold EN (2006) Systematics, biogeography, and evolution of Hemidactylus geckos (Reptilia: Gekkonidae) elucidated using mitochondrial DNA sequences. Mol Phylogenet Evol 38:531–545

    CAS  Google Scholar 

  10. Carranza S, Arnold EN (2012) A review of the geckos of the genus Hemidactylus (Squamata: Gekkonidae) from Oman based on morphology, mitochondrial and nuclear data, with descriptions of eight new species. Zootaxa 3378:1–95

    Google Scholar 

  11. Cheke AS, Hume JP (2008) Lost land of the dodo, the ecological history of the Mascarene Islands. Yale University Press, New Haven

    Google Scholar 

  12. Cheung C, De Vantier L (2006) Socotra. A natural history of the islands and their people. Odyssey Publications, Hong Kong

    Google Scholar 

  13. Cox NA, Mallon D, Bowles P, Els J, Tognelli MF (2012) The Conservation Status and Distribution of Reptiles of the Arabian Peninsula. IUCN, and Sharjah, UAE Environment and Protected Areas Authority, Cambridge

    Google Scholar 

  14. Crottini A, Madsen O, Poux C, Strauß A, Vieites DR, Vences M (2012) Vertebrate time-tree elucidates the biogeographic pattern of a major biotic change around the K-T boundary in Madagascar. Proc Natl Acad Sci USA 109:5358–5363

    CAS  Google Scholar 

  15. Fasola M, Ahmed Saeed, Pella F (2014) Biodiversity, the main asset of Soqotra, can it survive the ongoing environmental trends? In: Attorre F (ed) Soqotra archipelago (Yemen): toward systemic and scientifically objective sustainability in development and conservation. Quaderni CEMAS, Edizioni Nuova Cultura, Roma, pp 51–64. https://doi.org/10.4458/0429

  16. Garcia-Porta J, Morales HE, Gómez-Díaz E, Sindaco R, Carranza S (2016a) Patterns of diversification in islands: a comparative study across three gecko genera in the Socotra Archipelago. Mol Phylogenet Evol 98:288–299

    Google Scholar 

  17. Garcia-Porta J, Šmíd J, Sol D, Fasola M, Carranza S (2016b) Testing the island effect on phenotypic diversification: insights from the Hemidactylus geckos of the Socotra Archipelago. Sci Rep 6:23729

    CAS  Google Scholar 

  18. Gómez-Diaz E, Sindaco R, Pupin F, Fasola M, Carranza S (2012) Origin and in situ diversification in Hemidactylus geckos of the Socotra Archipelago. Mol Ecol 21:4074–4092

    Google Scholar 

  19. Heyer RW, Donnelly MA, McDiarmid RW, Hayek LAC, Foster MS (1994) Measuring and monitoring Biological Diversity. Standard Methods for Amphibians, 1. Smithsonian University Press, Washington

    Google Scholar 

  20. Kapli P, Lymberakis P, Poulakakis N, Mantziou G, Parmakelis A, Mylonas M (2008) Molecular phylogeny of three Mesalina (Reptilia: Lacertidae) species (M. guttulata, M. brevirostris and M. bahaeldini) from North Africa and the Middle East: another case of paraphyly? Mol Phylogenet Evol 49:102–110

    CAS  Google Scholar 

  21. Kapli P, Lymberakis P, Crochet PA, Geniez P, Brito JC, Almutairi M, Poulakakis N (2015) Historical biogeography of the lacertid lizard Mesalina in North Africa and the Middle East. J Biogeogr 42:267–279

    Google Scholar 

  22. Kornilios P, Giokas S, Lymberakis P, Sindaco R (2013) Phylogenetic position, origin and biogeography of Palearctic and Socotran blind-snakes (Serpentes: Typhlopidae). Mol Phylogenet Evol 68:35–41

    CAS  Google Scholar 

  23. Macey JR, Kuehl JV, Larson A, Robinson MD, Ugurtas IH, Ananjeva NB, Rahman H, Javed HI, Osman RM, Doumma A, Papenfuss TJ (2008) Socotra Island the forgotten fragment of Gondwana: unmasking chameleon lizard history with complete mitochondrial genomic data. Mol Phylogenet Evol 49:1015–1018

    CAS  Google Scholar 

  24. Martín N, Martínez S, Pujol-Buxó E, Vinolas A, Llorente GA, Sanpera C, Santos X (2017) Stable isotopes and diet uncover trophic-niche divergence and ecological diversification processes of endemic reptiles on Socotra Island. Zool Anz 267:69–81

    Google Scholar 

  25. Nagy ZT, Joger U, Wink M, Glaw F, Vences M (2003) Multiple colonization of Madagascar and Socotra by colubrid snakes: evidence from nuclear and mitochondrial gene phylogenies. Proc R Soc Lond B Biol Sci 270:2613–2621

    Google Scholar 

  26. Nagy ZT, Lawson R, Joger U, Wink M (2004) Molecular systematics of racers, whipsnakes and relatives (Reptilia: Colubridae) using mitochondrial and nuclear markers. J Zool Syst Evol Res 42:223–233

    Google Scholar 

  27. Peutz N (2018) Islands of heritage conservation and transformation in Yemen. Stanford University Press, Palo Alto

    Google Scholar 

  28. Phillott AD, Rees AF (eds) (2018) Sea Turtles in the Middle East and South Asia Region: MTSG Annual Regional Report 2018. Draft Report of the IUCN-SSC Marine Turtle Specialist Group

  29. Razzetti E, Sindaco R, Grieco C, Pella F, Ziliani U, Pupin F, Riservato E, Pellitteri-Rosa D, Butikofer L, Suleiman AS, Ba A-A, Carugati C, Boncompagni E, Fasola M (2011) Annotated checklist and distribution of the Socotran archipelago herpetofauna (Reptilia). Zootaxa 2826:1–44

    Google Scholar 

  30. Rösler H, Wranik W (2006) The reptiles of the Socotra archipelago with special remarks on the slender blind snakes (Leptotyphlopidae: Leptotyphlops). In: Herpetologia Bonnensis II. Proceedings of the 13th Congress of the Societas Europaea Herpetologica. pp 125–128

  31. Rösler H, Wranik W (2007) Bemerkungen zur Biologie sowie Haltung und Vermehrung des Sokotra-Riesengeckos, Haemodracon riebeckii (Peters, 1882). Der Zoologische Garten 77:59–83. https://doi.org/10.1016/j.zoolgart.2007.08.001

    Article  Google Scholar 

  32. Sancho V, Vasconcelos R, Llorente G, Santos X (2017) Morphological differentiation of the complex Pristurus sokotranus (Squamata: Sphaerodactylidae) from Socotra (Yemen). Zootaxa 4324:63–84

    Google Scholar 

  33. Siliceo I, Diaz JA (2010) A comparative study of clutch size, range size, and the conservation status of island vs.mainland lacertid lizards. Biol Conserv 14:2601–2608

    Google Scholar 

  34. Simó-Riudalbas M, Tamar K, Šmíd J, Mitsi P, Sindaco R, Chirio L, Carranza S (2019) Biogeography of Mesalina (Reptilia: Lacertidae), with special emphasis on the Mesalina adramitana group from Arabia and the Socotra Archipelago. Mol Phylogenet Evol 137:300–312

    Google Scholar 

  35. Sindaco R, Ziliani U, Razzetti E, Carugati C, Grieco C, Pupin F, Pella F, Fasola M (2009) A misunderstood new gecko of the genus Hemidactylus from Socotra Island, Yemen (Reptilia: Squamata: Gekkonidae). Acta Herpetol 4:83–98

    Google Scholar 

  36. Sindaco R, Metallinou M, Pupin F, Fasola M, Carranza S (2012) Forgotten in the ocean: systematics, biogeography and evolution of the Trachylepis skinks of the Socotra Archipelago. Zoolog Scr 41:346–362

    Google Scholar 

  37. Sinervo B, Méndez-de-la-Cruz F, Miles DB, Heulin B, Bastiaans E, Villagrán-Santa Cruz M, Lara-Resendiz R, Martínez-Méndez N, Calderón-Espinosa ML, Meza-Lázaro RN, Gadsden H, Avila LJ, Morando M, De la Riva IJ, Sepulveda PV, Duarte Rocha CF, Ibargüengoytía N, Aguilar Puntriano C, Massot M, Lepetz V, Oksanen TA, Chapple DG, Bauer AM, Branch WR, Clobert J, Sites JW Jr (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894–899

    CAS  Google Scholar 

  38. Šmíd J, Carranza S, Kratochvíl L, Gvoždík V, Nasher AK, Moravec J (2013) Out of Arabia: a complex biogeographic history of multiple vicariance and dispersal events in the gecko genus Hemidactylus (Reptilia: Gekkonidae). PLoS ONE 8:e64018

    Google Scholar 

  39. Tamar K, Simó-Riudalbas M, Garcia-Porta J, Llorente G, Vasconcelos R, Carranza S (2019) An integrative study of island diversification: Insights from the endemic Haemodracon geckos of the Socotra Archipelago. Mol Phylogenet Evol 133:166–175

    Google Scholar 

  40. Tilbury C (2018) Chameleons of Africa, an Atlas. Including the chameleons of Europe, the Middle East and Asia. Edition Chimaira, Frankfurt am Main, p 643

    Google Scholar 

  41. Tolley KA, Townsend TM, Vences M (2013) Large-scale phylogeny of chameleons suggests African origins and Eocene diversification. Proc R Soc Lond B Biol Sci 280:20130184

    Google Scholar 

  42. UNESCO World Heritage Committee (2010) Socotra Archipelago. United Nations - UNESCO World Heritage Centre v.3.0. http://whc.unesco.org/en/list/1263

  43. Van Damme K (2009) Socotra Archipelago. In: Gillespie RG, Clague DA (eds) Encyclopedia of islands. University of California Press, Berkeley and Los Angeles, pp 846–851

    Google Scholar 

  44. Van Damme K, Banfield L (2011) Past and present human impacts on the biodiversity of Socotra Island (Yemen): implications for future conservation. Zool Middle East 54:31–88

    Google Scholar 

  45. Van Damme K, Benda P, Van Damme D, De Geest P, Hajdas I (2018) The first vertebrate fossil from Socotra Island (Yemen) is an early Holocene Egyptian fruit bat. J Nat Hist 52:2001–2024

    Google Scholar 

  46. Vasconcelos R, Carranza S (2014) Systematics and biogeography of Hemidactylus homoeolepis Blanford, 1881 (Squamata: Gekkonidae), with the description of a new species from Arabia. Zootaxa 3835:501–527

    Google Scholar 

  47. Vasconcelos R, Montero-Mendieta S, Simó-Riudalbas M, Sindaco R, Santos X, Fasola M, Llorente G, Razzetti E, Carranza S (2016) Unexpectedly high levels of cryptic diversity uncovered by a complete DNA barcoding of reptiles of the Socotra Archipelago. PLoS ONE. https://doi.org/10.1371/journal.pone.0200830

    Article  Google Scholar 

  48. Vasconcelos R, Razgour O, Tarroso P, Fasola M, Carranza S, Alves PC (2018) Combining molecular and landscape tools for targeting evolutionary processes in reserve design: an approach for islands. PLoS ONE 13(7):e0200830

    Google Scholar 

  49. Vasconcelos R, Pujol-Buxó E, Llorente G, Saeed A, Carranza S (2020) Micro-Hotspots for conservation: an umbrella tree species for the unique Socotran reptile fauna. Forests 11:353

    Google Scholar 

  50. Wilson DE, Mittermeier RA (eds) (2018) Handbook of the mammals of the world, vol 8. Lynx Edicions, Barcelona

    Google Scholar 

  51. Wranik W (2003) Fauna of the Socotra Arcipelago. Field Guide. With contributions from Al-Saghier OS, Aspinall S, Porter RF, Rösler H. Rostock, Germany

  52. Yousefkhani SSH, Marin M, Gabriel MD, Rastegar-Pouyani N, Rastegar-Pouyani E (2015) A bibliographic recompilation of the genus Mesalina Gray, 1838 (Sauria: Lacertidae) with a key to the species. Russ J Herpetol 22:23–34

    Google Scholar 

Download references

Acknowledgements

Our field surveys in Socotra were accomplished within the programs “Socotra Conservation and Development” by United Nations Development Program, and “Capacity Development for Soqotra Archipelago Conservation” by the Italian International Cooperation. RV was supported by a contract from ‘Fundação para a Ciência e a Tecnologia’ (FCT), I.P. national funds from ‘Norma transitória’ (DL57/2016/CP1440/CT0002). We are grateful for their support to Akmed Abdulrahman Fadel Al-Eryani, Minister of Water and Environment at the time of our fieldwork in Socotra 2007–2010, and to Ahmed Saeed Suleiman of the Socotra Environment Protection Agency. Several Yemeni and European colleagues and friends participated to the field surveys, Abdul Raqeb, Yaya Saleh Saeed, Salem Hamdiah, Abubakar Salim, Badar Awadh Al-Aseily, Ahmed Saeed Saif, Eleonora Boncompagni, Luca Butikofer, Caterina Carugati, Cristina Grieco, Francesca Pella, Fabio Pupin, Elisa Riservato, Oreste Sacchi and Xavier Santos.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Mauro Fasola.

Ethics declarations

Ethical statement

The authors declare that they have no conflict of interest. This article does not contain any studies with human subjects. Data collection throughout our surveys were performed with permission by the Yemeni Minister of Water and Environment and in collaboration with the Environment Protection Agency of Socotra.

Additional information

Publisher's Note

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

This paper belongs to a Topical Collection “Twenty years of biodiversity research and nature conservation in the Socotra Archipelago” edited by Fabio Attorre and Kay Van Damme, conceived at the 18th Friends of Socotra Conference, 26–29 September, 2019, Orto Botanico di Palermo, Palermo, Italy”.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fasola, M., Razzetti, E., Sindaco, R. et al. Ecological preferences of the endemic reptile community of Socotra. Rend. Fis. Acc. Lincei (2020). https://doi.org/10.1007/s12210-020-00922-w

Download citation

Keywords

  • Indian Ocean
  • Islands
  • Geckos
  • Endemism
  • Habitat use
  • Activity pattern
  • Ecological niche