Repeated evolution of flightlessness in Dryolimnas rails (Aves: Rallidae) after extinction and recolonization on Aldabra

Repeated evolution of flightlessness in Dryolimnas rails (Aves: Rallidae) after extinction and... Abstract The Aldabra rail, Dryolimnas cuvieri subsp. aldabranus, endemic to the Aldabra Atoll, Seychelles, is the last surviving flightless bird in the Indian Ocean. Aldabra has undergone at least one major, total inundation event during an Upper Pleistocene (Tarantian age) sea-level high-stand, resulting in the loss of all terrestrial fauna. A flightless Dryolimnas has been identified from two temporally separated Aldabran fossil localities, deposited before and after the inundation event, providing irrefutable evidence that a member of Rallidae colonized the atoll, most likely from Madagascar, and became flightless independently on each occasion. Fossil evidence presented here is unique for Rallidae and epitomizes the ability of birds from this clade to successfully colonize isolated islands and evolve flightlessness on multiple occasions. Aldabra Atoll, fossil, flightless, extinction, sea-level rise, recolonization INTRODUCTION The white-throated rail, Dryolimnas cuvieri (Pucheran, 1845), is indigenous to islands in the south-western Indian Ocean and occurs widely throughout the region (Fig. 1) where it is known to include three subspecies. Volant D. c. subsp. cuvieri is found today on Madagascar and Mayotte (Safford & Hawkins, 2013), with a totally flightless derivative on Aldabra, D. c. subsp. aldabranus (Günther, 1879), the last surviving flightless rail in the Indian Ocean (Stoddart & Wright, 1967), and a poorly volant/flightless subspecies, D. c. subsp. abbotti (Ridgway, 1894) formerly on Assumption (Nicoll, 1908), which became extinct between 1907 and 1937 (Safford & Hawkins, 2013; Hume, 2017). Possibly distinct, but now extinct, rail populations reputedly occurred on Ile aux Cèdres (Aldabra), Cosmoledo Atoll and Astove Island (Collar, 1993) (Figs 1, 2), but no specimens were collected to confirm their status. However, a distinct Dryolimnas population on the tiny islet of Ile aux Cèdres in the Aldabra lagoon appears unlikely. In addition, two Dryolimnas species once inhabited the Mascarenes: the large, flightless Réunion rail, D. augustiMourer-Chauviré et al., 1999, which survived until at least the end of the 17th century (Mourer-Chauviré et al., 1999), and a probably flightless, undescribed Dryolimnas from Mauritius that was last recorded in 1638 (Hume, 2013, 2017). Figure 1. View largeDownload slide Outline map of the south-western Indian Ocean showing the distribution of Dryolimnas: Dryolimnas c. cuvieri; D. c. aldabranus; †D. c. abbotti; †D. augusti; †D. sp. † = extinct. Figure 1. View largeDownload slide Outline map of the south-western Indian Ocean showing the distribution of Dryolimnas: Dryolimnas c. cuvieri; D. c. aldabranus; †D. c. abbotti; †D. augusti; †D. sp. † = extinct. Figure 2. View largeDownload slide Outline map of Aldabra Atoll indicating the fossil localities discussed in the text. Adapted from Hume et al. (2018). Figure 2. View largeDownload slide Outline map of Aldabra Atoll indicating the fossil localities discussed in the text. Adapted from Hume et al. (2018). The discovery of fossil remains of a flightless Dryolimnas (two humeri) at Bassin Cabri on Ile Picard confirms the presence of the bird on Aldabra during the Middle Pleistocene (Chibanian age) to the Upper Pleistocene (Tarantian age; Hume et al., 2018) (Fig. 2). The absolute maximum age of the Aldabra Atoll is unknown, but inferences made from sea-level high-stands dating back 400 000 years before present (YBP) show that the Aldabra platform was subject to at least one total inundation event around 340 000 YBP, with possibly two others at 240 000 and 200 000 YBP, respectively (Braithwaite et al., 1973; Braithwaite, 1984) (Fig. 3). An undated limestone depositional sequence (Picard Calcarenites) exposed on present-day Ile Picard must be in excess of 136 000 YBP, as the younger, overlying and island-wide Aldabra Limestone has been dated from Ile Picard deposits between 136 000 (Middle Pleistocene) and 118 000 (Upper Pleistocene) YBP ± 9000 (~127 000+) (Thomson & Walton, 1972; Braithwaite et al., 1973) (Fig. 3), which represents the most recent complete inundation event. The Bassin Cabri cavity-fill fossil material accumulated during this period (for a detailed depositional history see: Braithwaite et al., 1973). After the deposition of the Aldabra Limestone, and with falling sea levels, terrestrial soils were created. A reptile-rich fossil deposit formed at Point Hodoul (inferred date ~100 000 YBP; Taylor et al., 1979), which included a distal tarsometatarsus of a Dryolimnas rail (Harrison & Walker, 1978). Figure 3. View largeDownload slide Figure showing the sea-level curve and possible inundation events that affected the Aldabra platform in the last 400 000+ YBP. The 118 000 and 136 000 YBP ± 9000 (~127 000+) sea-level high-stand separates the Ile Picard and Point Hodoul fossil localities. Adapted from Perry & Hsu (2000) and Andreas et al. (2012). Figure 3. View largeDownload slide Figure showing the sea-level curve and possible inundation events that affected the Aldabra platform in the last 400 000+ YBP. The 118 000 and 136 000 YBP ± 9000 (~127 000+) sea-level high-stand separates the Ile Picard and Point Hodoul fossil localities. Adapted from Perry & Hsu (2000) and Andreas et al. (2012). MATERIAL AND METHODS Specimens Two humeri held at the Smithsonian Institution National Museum of Natural History (USNM) and a distal tarsometatarsus held at the Natural History Museum, London (NHMUK) of Pleistocene Dryolimnas cuvieri were compared with modern specimens held at the Natural History Museum, Tring (NHMUK) of D. c. cuvieri, D. c. aldabranus and a unique skeleton of the extinct, D. c. abbotti (Supporting Information, Tables S1, S2). Morphometric analysis Measurements were taken using a dial calliper and rounded to the nearest 0.1mm. Only humeri and distal tarsometatarsi were available, so measurements of total length, proximal width, proximal depth, shaft width, shaft depth, distal width and distal depth of humerus (Supporting Information, Table S1) and distal width, distal depth and greatest depths taken proximal to trochlea. Metatarsi II were used for tarsometatarsus (Supporting Information, Table S2). Anatomical terminology follows Baumal & Witmer (1993). RESULTS Morphology The rail humeri from Bassin Cabri are almost undifferentiated from modern D. c. aldabranus, other than being more robust proximally, with the crista bicipitalis more expanded, the shaft more robust and straighter, and the epicondylus dorsalis less pronounced. Like D. c. aldabranus, it also differs considerably in size from D. c. cuvieri and D. c. abbotti (Fig. 4; Supporting Information, Tables S1, S3). In the few morphometrics available from the tarsometatarsus, the Point Hodoul specimen shows a very similar morphology to D. c. aldabranus and D. c. abbotti compared with nominate, with the foramen vasculare distale more deeply situated and further distad, the incisura intertrochlearis more open and trochlea. metatarsi II larger and directed further mediad (Fig. 5; Supporting Information, Tables S2, S4); characters indicative of flightlessness (Olson, 1977). The more robust distal end of the tarsometatarsus in the Pleistocene specimen, together with the depth of the shaft proximal to the trochlea also greater than in nominate, suggests that Dryolimnas had become more terrestrial and flightless. Figure 4. View largeDownload slide A comparison of humeri (left side) of Dryolimnas used in this study. From left to right: D. cuvieri aldabranus NHMUK S/1989.38.7 ♂; D. cuvieri (Upper Pleistocene) USNM UJP79 unsexed; D. c. abbotti NHMUK 1910.4.8.1 unsexed; D. c. cuvieri NHMUK 1897.5.10.47 unsexed. Scale bar = 10mm. From Hume et al. (2018). Figure 4. View largeDownload slide A comparison of humeri (left side) of Dryolimnas used in this study. From left to right: D. cuvieri aldabranus NHMUK S/1989.38.7 ♂; D. cuvieri (Upper Pleistocene) USNM UJP79 unsexed; D. c. abbotti NHMUK 1910.4.8.1 unsexed; D. c. cuvieri NHMUK 1897.5.10.47 unsexed. Scale bar = 10mm. From Hume et al. (2018). Figure 5. View largeDownload slide A comparison of tarsometatarsi (right side) of Dryolimnas used in this study. From left to right: D. cuvieri (Upper Pleistocene) NHMUK A4380 unsexed; D. cuvieri aldabranus NHMUK S/1989.38.7 ♂; D. c. abbotti NHMUK 1910.4.8.1 unsexed; D. c. cuvieri NHMUK 1897.5.10.47 unsexed. Scale bar = 10mm. Figure 5. View largeDownload slide A comparison of tarsometatarsi (right side) of Dryolimnas used in this study. From left to right: D. cuvieri (Upper Pleistocene) NHMUK A4380 unsexed; D. cuvieri aldabranus NHMUK S/1989.38.7 ♂; D. c. abbotti NHMUK 1910.4.8.1 unsexed; D. c. cuvieri NHMUK 1897.5.10.47 unsexed. Scale bar = 10mm. DISCUSSION The complete inundation of the Aldabra Atoll during deposition of the Aldabra Limestone resulted in the extinction of the endemic Aldabra petrel Pterodroma kurodai Harrison & Walker, 1978, Aldabra duck Aldabranus cabri Harrison & Walker, 1978 and loss of other bird taxa, including the flightless Dryolimnas rail (Harrison & Walker, 1978; Taylor et al., 1979). A number of reptiles also disappeared, including an endemic horned crocodile Aldabrachampsus dilophus Brochu, 2006, the giant tortoise Aldabrachelys cf. gigantea Loveridge & Williams, 1957, an Oplurus iguana and terrestrial skinks (Arnold, 1979). At the younger Point Hodoul fossil deposit, the occurrence of giant tortoise, iguana, skinks and Dryolimnas show that the atoll was seemingly rapidly recolonized on re-emergence, at least from 100 000 YBP (Taylor et al., 1979). The presence of Dryolimnas at both deposits requires explanation. The Bassin Cabri humeri indicate the rail was already flightless at ~127 000+ YBP during the Middle Pleistocene (Fig. 6); therefore, it must have disappeared, along with the other terrestrial fauna, when the atoll was completely submerged (Thomson & Walton, 1972; Taylor et al., 1979). Furthermore, characters of the tarsometatarsus in the Pleistocene specimen suggest that it had evolved a degree of flightlessness at least comparable with D. c. abbotti (Harrison & Walker, 1978), being shorter and more robust than the nominate and D. c. aldabranus (Fig. 7). This, and its presence on Aldabra today, provides irrefutable evidence that Dryolimnas subsequently recolonized Aldabra after inundation and became flightless for a second time. This scenario may seem surprising, but rails are known to be persistent colonizers of isolated islands and can evolve flightlessness rapidly if suitable conditions exist (Olson, 1977). Therefore, it is likely that the dispersal of nominate Dryolimnas from Madagascar to remote Aldabra occurred on multiple occasions, as did giant tortoises (Taylor et al., 1979). The Point Hodoul fossil record shows that the giant tortoise, iguana, a number of lizard taxa and Dryolimnas successfully recolonized the atoll (Hume et al. 2018), but the iguana and most other lizards subsequently perished. Based on the geological record (Braithwaite et al., 1973), this extinction event appears to be unrelated to inundation and may have been the result of introduced black rats Rattus rattus (Linneaus, 1758), which were present on Aldabra in 1890 (Cheke, 2010) but no doubt arrived much earlier. Figure 6. View largeDownload slide Density plots of measurements (mm) of the humerus of Dryolimnas, showing that Pleistocene Dryolimnas cuvieri nestles in with the flightless species. Abbreviations: TL, total length; PW, proximal width; PD, proximal depth; SW, shaft width; SD, shaft depth; DW, distal width; DD, distal depth; (n), number of specimens; (m), mean; SD, Standard Deviation. Figure 6. View largeDownload slide Density plots of measurements (mm) of the humerus of Dryolimnas, showing that Pleistocene Dryolimnas cuvieri nestles in with the flightless species. Abbreviations: TL, total length; PW, proximal width; PD, proximal depth; SW, shaft width; SD, shaft depth; DW, distal width; DD, distal depth; (n), number of specimens; (m), mean; SD, Standard Deviation. Figure 7. View largeDownload slide Density plots of measurements (mm) of the tarsometatarsus of Dryolimnas, showing that Pleistocene Dryolimnas cuvieri approximates flightless species. Abbreviations: DW, distal width; DD, distal depth; TMD, greatest depth taken proximal to trochlea. metatarsi II; (n), number of specimens; (m), mean; SD, Standard Deviation. Figure 7. View largeDownload slide Density plots of measurements (mm) of the tarsometatarsus of Dryolimnas, showing that Pleistocene Dryolimnas cuvieri approximates flightless species. Abbreviations: DW, distal width; DD, distal depth; TMD, greatest depth taken proximal to trochlea. metatarsi II; (n), number of specimens; (m), mean; SD, Standard Deviation. Only relatively few taxa from the Middle to Upper Pleistocene fossil deposits on Aldabra survived into the Holocene. Of those that did, apart from breeding sea birds, the most notable are adept open-water travellers, including giant tortoises (by floating) (Gerlach et al., 2006) and Dryolimnas rails (periodic, long-distance flight dispersal) (Wanless & Hockey, 2008). Evidence of multiple avian colonization events with recurring flightlessness are extremely rare in the fossil record (e.g. Olson & James, 1991; Fulton et al., 2012), especially on smaller oceanic islands where long-term preservation of fossiliferous material is generally poor. We know of no other example in Rallidae, or of birds in general, that demonstrates this phenomenon so evidently. Only on Aldabra, which has the oldest palaeontological record of any oceanic island in the Indian Ocean region (Thomson & Walton, 1972), is fossil evidence available that demonstrates the effects of changing sea levels on extinction and recolonization events. Conditions were such on Aldabra, the most important being the absence of terrestrial predators and competing mammals, that a Dryolimnas rail was able to evolve flightlessness independently on each occasion. ACKNOWLEDGEMENTS We thank Robert Prŷs-Jones, Julia Heinen, Anthony Cheke and an anonymous reviewer for comments that helped improve this paper, and we especially thank Julia Heinen for providing the excellent statistical figures. We thank Storrs Olson, Helen James, Jennifer Strotman and Mark Florence (USNM) for the long-term loan of the John Becker Aldabra material. We thank Sandra Chapman and Lorna Steel (NHMUK) for access to material in their care; Harry Taylor (NHMUK) for photography and Richard Hing (University of Portsmouth) for some fossil preparation. We especially thank the Percy Sladen Centenary Fund whose financial support made this research possible. SUPPORTING INFORMATION Supporting information may be found in the online version of this article at the publisher’s web-site. Table S1. Summary statistics for measurements (mm) of the humerus of Dryolimnas. Table S2. Summary statistics for measurements (mm) of the tarsometatarsus of Dryolimnas. TableS3. Raw measurements (mm) of the humerus of Dryolimnas. Table S4. Raw measurements (mm) of the tarsometatarsus of Dryolimnas. REFERENCES Andreas P , Reijmer JJG , Fürstenau J , Kinkel H , Betzler C . 2012 . Relationship between Late Pleistocene sea-level variations, carbonate platform morphology and aragonite production (Maldives, Indian Ocean) . Sedimentology 59 : 1640 – 1658 . Google Scholar Crossref Search ADS Arnold EN . 1979 . Fossil reptiles from Aldabra Atoll, Indian Ocean . Bulletin of the British Museum (Natural History), Zoology 29 : 85 – 116 . Baumel JJ , Witmer LM . 1993 . Osteologia. In: Baumel JJ , King AS , Breazile JE , Evans HE , Vanden Berge JC , eds. Handbook of avian anatomy: nomina anatomica avium , 2 nd edn. Cambridge : Publications of the Nuttall Ornithological Club , 45 – 132 . Braithwaite CJR . 1984 . Geology of the Seychelles. In: Stoddart DR , ed. Biogeography and ecology of the Seychelles Islands . The Hague : Dr W. Junk Publishers , 17 – 38 . Braithwaite CJR , Taylor JD , Kennedy WJ . 1973 . The evolution of an atoll: the depositional and erosional history of Aldabra . Philosophical Transactions of the Royal Society of London B 266 : 307 – 340 . Google Scholar Crossref Search ADS Brochu CA . 2006 . A new miniature horned crocodile from the Quaternary of Aldabra Atoll, western Indian Ocean . Copeia 2 : 149 – 158 . Google Scholar Crossref Search ADS Cheke A . 2010 . The timing of arrival of humans and their commensal animals on Western Indian Ocean oceanic Islands . Phelsuma 18 : 38 – 69 . Collar NJ . 1993 . The conservation status in 1982 of the Aldabran white-throated rail Dryolimnas cuvieri aldabranus . Bird Conservation International 3 : 299 – 305 . Google Scholar Crossref Search ADS Fulton TL , Letts B , Shapiro B . 2012 . Multiple losses of flight and recent speciation in steamer ducks . Proceedings of the Royal Society B, Biological Sciences 279 : 2339 – 2346 . Google Scholar Crossref Search ADS Gerlach J , Muir C , Richmond MD . 2006 . The first substantiated case of trans-oceanic tortoise dispersal . Journal of Natural History 40 : 2403 – 2408 . Google Scholar Crossref Search ADS Günther A . 1879 . On the occurrence of a land-rail (Rallus) in the Island of Aldabra . Annals and Magazine of Natural History 3 : 164 – 168 . Google Scholar Crossref Search ADS Harrison CJO , Walker CA . 1978 . Pleistocene bird remains from Aldabra Atoll, Indian Ocean . Journal of Natural History 12 : 7 – 14 . Google Scholar Crossref Search ADS Hume JP . 2013 . A synopsis of the pre-human avifauna of the Mascarene Islands. In: Göhlich UB , Kroh A , eds. Proceedings of the 8th international meeting of the Society of avian paleontology and evolution . Vienna : Natural History Museum , 195 – 237 . Hume JP . 2017 . Extinct birds , 2 nd edn. London : Christopher Helm . Hume JP , Martill D , Hing R . 2018 . A palaeontological review of Aldabra Atoll, Aldabra Group, Seychelles . PlosOne . doi: https://doi.org/10.1371/journal.pone.0192675 . Perry CA , Hsu KJ . 2000 . Geophysical, archaeological, and historical evidence support a solar-output model for climate change . PNAS 97 : 12433 – 12438 . Google Scholar Crossref Search ADS PubMed Loveridge A , Williams EE . 1957 . Revision of the African tortoises and turtles of the suborder Cryptodira . Bulletin of the Museum of Comparative Zoology, Harvard 115 : 161 – 557 . Mourer-Chauviré C , Bour R , Ribes S , Moutou F . 1999 . The avifauna of Réunion Island (Mascarene Islands) at the time of the arrival of the first Europeans . Smithsonian Contributions to Paleobiology 89 : 1 – 38 . Nicoll MJ . 1908 . Three voyages of a naturalist . London : Witherby and Co . Olson SL . 1977 . A synopsis of the fossil Rallidae. In: Ripley SD , ed. Rails of the world. A monograph of the family Rallidae . Boston : David R. Godine , 338 – 378 . Olson SL , James HF . 1991 . Descriptions of 32 new species of birds from the Hawaiian Islands: part 1, non-Passeriformes . Ornithological Monographs 45 : 1 – 88 . Google Scholar Crossref Search ADS Pucheran MLD . 1845 . Notes sur quelques espèces Madécasses de l’ordre des Échassiers . Revue Zoologique par la Société Cuvierienne 1845 : 277 – 280 . Ridgway R . 1894 . Descriptions of some new birds from Aldabra, Assumption, and Gloriosa Islands, collected by Dr W. L. Abbott . Proceedings of the United States National Museum 17 : 371 – 373 . Google Scholar Crossref Search ADS Safford R , Hawkins F . 2013 . Birds of Africa, vol. VIII: the Malagasy region . London : Christopher Helm . Stoddart DR , Wright CA . 1967 . Geography and ecology of Aldabra Atoll . Atoll Research Bulletin 118 : 11 – 52 . Taylor JD , Braithwaite CJR , Peake JF , Arnold EN . 1979 . Terrestrial faunas and habitats of Aldabra during the Late Pleistocene . Philosophical Transactions of the Royal Society of London B 286 : 47 – 66 . Google Scholar Crossref Search ADS Thomson J , Walton A . 1972 . Redetermination of chronology of Aldabra Atoll by 230Th/234U dating . Nature 240 : 145 – 146 . Google Scholar Crossref Search ADS Wanless RM , Hockey PAR . 2008 . Natural behaviour of the Aldabra Rail (Dryolimnas [cuvieri] aldabranus) . Wilson Journal of Ornithology 120 : 50 – 61 . Google Scholar Crossref Search ADS © 2019 The Linnean Society of London, Zoological Journal of the Linnean Society This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Zoological Journal of the Linnean Society Oxford University Press

Repeated evolution of flightlessness in Dryolimnas rails (Aves: Rallidae) after extinction and recolonization on Aldabra

Loading next page...
 
/lp/ou-press/repeated-evolution-of-flightlessness-in-dryolimnas-rails-aves-rallidae-tVFzh8I5pa
Publisher
Oxford University Press
Copyright
© 2019 The Linnean Society of London, Zoological Journal of the Linnean Society
ISSN
0024-4082
eISSN
1096-3642
DOI
10.1093/zoolinnean/zlz018
Publisher site
See Article on Publisher Site

Abstract

Abstract The Aldabra rail, Dryolimnas cuvieri subsp. aldabranus, endemic to the Aldabra Atoll, Seychelles, is the last surviving flightless bird in the Indian Ocean. Aldabra has undergone at least one major, total inundation event during an Upper Pleistocene (Tarantian age) sea-level high-stand, resulting in the loss of all terrestrial fauna. A flightless Dryolimnas has been identified from two temporally separated Aldabran fossil localities, deposited before and after the inundation event, providing irrefutable evidence that a member of Rallidae colonized the atoll, most likely from Madagascar, and became flightless independently on each occasion. Fossil evidence presented here is unique for Rallidae and epitomizes the ability of birds from this clade to successfully colonize isolated islands and evolve flightlessness on multiple occasions. Aldabra Atoll, fossil, flightless, extinction, sea-level rise, recolonization INTRODUCTION The white-throated rail, Dryolimnas cuvieri (Pucheran, 1845), is indigenous to islands in the south-western Indian Ocean and occurs widely throughout the region (Fig. 1) where it is known to include three subspecies. Volant D. c. subsp. cuvieri is found today on Madagascar and Mayotte (Safford & Hawkins, 2013), with a totally flightless derivative on Aldabra, D. c. subsp. aldabranus (Günther, 1879), the last surviving flightless rail in the Indian Ocean (Stoddart & Wright, 1967), and a poorly volant/flightless subspecies, D. c. subsp. abbotti (Ridgway, 1894) formerly on Assumption (Nicoll, 1908), which became extinct between 1907 and 1937 (Safford & Hawkins, 2013; Hume, 2017). Possibly distinct, but now extinct, rail populations reputedly occurred on Ile aux Cèdres (Aldabra), Cosmoledo Atoll and Astove Island (Collar, 1993) (Figs 1, 2), but no specimens were collected to confirm their status. However, a distinct Dryolimnas population on the tiny islet of Ile aux Cèdres in the Aldabra lagoon appears unlikely. In addition, two Dryolimnas species once inhabited the Mascarenes: the large, flightless Réunion rail, D. augustiMourer-Chauviré et al., 1999, which survived until at least the end of the 17th century (Mourer-Chauviré et al., 1999), and a probably flightless, undescribed Dryolimnas from Mauritius that was last recorded in 1638 (Hume, 2013, 2017). Figure 1. View largeDownload slide Outline map of the south-western Indian Ocean showing the distribution of Dryolimnas: Dryolimnas c. cuvieri; D. c. aldabranus; †D. c. abbotti; †D. augusti; †D. sp. † = extinct. Figure 1. View largeDownload slide Outline map of the south-western Indian Ocean showing the distribution of Dryolimnas: Dryolimnas c. cuvieri; D. c. aldabranus; †D. c. abbotti; †D. augusti; †D. sp. † = extinct. Figure 2. View largeDownload slide Outline map of Aldabra Atoll indicating the fossil localities discussed in the text. Adapted from Hume et al. (2018). Figure 2. View largeDownload slide Outline map of Aldabra Atoll indicating the fossil localities discussed in the text. Adapted from Hume et al. (2018). The discovery of fossil remains of a flightless Dryolimnas (two humeri) at Bassin Cabri on Ile Picard confirms the presence of the bird on Aldabra during the Middle Pleistocene (Chibanian age) to the Upper Pleistocene (Tarantian age; Hume et al., 2018) (Fig. 2). The absolute maximum age of the Aldabra Atoll is unknown, but inferences made from sea-level high-stands dating back 400 000 years before present (YBP) show that the Aldabra platform was subject to at least one total inundation event around 340 000 YBP, with possibly two others at 240 000 and 200 000 YBP, respectively (Braithwaite et al., 1973; Braithwaite, 1984) (Fig. 3). An undated limestone depositional sequence (Picard Calcarenites) exposed on present-day Ile Picard must be in excess of 136 000 YBP, as the younger, overlying and island-wide Aldabra Limestone has been dated from Ile Picard deposits between 136 000 (Middle Pleistocene) and 118 000 (Upper Pleistocene) YBP ± 9000 (~127 000+) (Thomson & Walton, 1972; Braithwaite et al., 1973) (Fig. 3), which represents the most recent complete inundation event. The Bassin Cabri cavity-fill fossil material accumulated during this period (for a detailed depositional history see: Braithwaite et al., 1973). After the deposition of the Aldabra Limestone, and with falling sea levels, terrestrial soils were created. A reptile-rich fossil deposit formed at Point Hodoul (inferred date ~100 000 YBP; Taylor et al., 1979), which included a distal tarsometatarsus of a Dryolimnas rail (Harrison & Walker, 1978). Figure 3. View largeDownload slide Figure showing the sea-level curve and possible inundation events that affected the Aldabra platform in the last 400 000+ YBP. The 118 000 and 136 000 YBP ± 9000 (~127 000+) sea-level high-stand separates the Ile Picard and Point Hodoul fossil localities. Adapted from Perry & Hsu (2000) and Andreas et al. (2012). Figure 3. View largeDownload slide Figure showing the sea-level curve and possible inundation events that affected the Aldabra platform in the last 400 000+ YBP. The 118 000 and 136 000 YBP ± 9000 (~127 000+) sea-level high-stand separates the Ile Picard and Point Hodoul fossil localities. Adapted from Perry & Hsu (2000) and Andreas et al. (2012). MATERIAL AND METHODS Specimens Two humeri held at the Smithsonian Institution National Museum of Natural History (USNM) and a distal tarsometatarsus held at the Natural History Museum, London (NHMUK) of Pleistocene Dryolimnas cuvieri were compared with modern specimens held at the Natural History Museum, Tring (NHMUK) of D. c. cuvieri, D. c. aldabranus and a unique skeleton of the extinct, D. c. abbotti (Supporting Information, Tables S1, S2). Morphometric analysis Measurements were taken using a dial calliper and rounded to the nearest 0.1mm. Only humeri and distal tarsometatarsi were available, so measurements of total length, proximal width, proximal depth, shaft width, shaft depth, distal width and distal depth of humerus (Supporting Information, Table S1) and distal width, distal depth and greatest depths taken proximal to trochlea. Metatarsi II were used for tarsometatarsus (Supporting Information, Table S2). Anatomical terminology follows Baumal & Witmer (1993). RESULTS Morphology The rail humeri from Bassin Cabri are almost undifferentiated from modern D. c. aldabranus, other than being more robust proximally, with the crista bicipitalis more expanded, the shaft more robust and straighter, and the epicondylus dorsalis less pronounced. Like D. c. aldabranus, it also differs considerably in size from D. c. cuvieri and D. c. abbotti (Fig. 4; Supporting Information, Tables S1, S3). In the few morphometrics available from the tarsometatarsus, the Point Hodoul specimen shows a very similar morphology to D. c. aldabranus and D. c. abbotti compared with nominate, with the foramen vasculare distale more deeply situated and further distad, the incisura intertrochlearis more open and trochlea. metatarsi II larger and directed further mediad (Fig. 5; Supporting Information, Tables S2, S4); characters indicative of flightlessness (Olson, 1977). The more robust distal end of the tarsometatarsus in the Pleistocene specimen, together with the depth of the shaft proximal to the trochlea also greater than in nominate, suggests that Dryolimnas had become more terrestrial and flightless. Figure 4. View largeDownload slide A comparison of humeri (left side) of Dryolimnas used in this study. From left to right: D. cuvieri aldabranus NHMUK S/1989.38.7 ♂; D. cuvieri (Upper Pleistocene) USNM UJP79 unsexed; D. c. abbotti NHMUK 1910.4.8.1 unsexed; D. c. cuvieri NHMUK 1897.5.10.47 unsexed. Scale bar = 10mm. From Hume et al. (2018). Figure 4. View largeDownload slide A comparison of humeri (left side) of Dryolimnas used in this study. From left to right: D. cuvieri aldabranus NHMUK S/1989.38.7 ♂; D. cuvieri (Upper Pleistocene) USNM UJP79 unsexed; D. c. abbotti NHMUK 1910.4.8.1 unsexed; D. c. cuvieri NHMUK 1897.5.10.47 unsexed. Scale bar = 10mm. From Hume et al. (2018). Figure 5. View largeDownload slide A comparison of tarsometatarsi (right side) of Dryolimnas used in this study. From left to right: D. cuvieri (Upper Pleistocene) NHMUK A4380 unsexed; D. cuvieri aldabranus NHMUK S/1989.38.7 ♂; D. c. abbotti NHMUK 1910.4.8.1 unsexed; D. c. cuvieri NHMUK 1897.5.10.47 unsexed. Scale bar = 10mm. Figure 5. View largeDownload slide A comparison of tarsometatarsi (right side) of Dryolimnas used in this study. From left to right: D. cuvieri (Upper Pleistocene) NHMUK A4380 unsexed; D. cuvieri aldabranus NHMUK S/1989.38.7 ♂; D. c. abbotti NHMUK 1910.4.8.1 unsexed; D. c. cuvieri NHMUK 1897.5.10.47 unsexed. Scale bar = 10mm. DISCUSSION The complete inundation of the Aldabra Atoll during deposition of the Aldabra Limestone resulted in the extinction of the endemic Aldabra petrel Pterodroma kurodai Harrison & Walker, 1978, Aldabra duck Aldabranus cabri Harrison & Walker, 1978 and loss of other bird taxa, including the flightless Dryolimnas rail (Harrison & Walker, 1978; Taylor et al., 1979). A number of reptiles also disappeared, including an endemic horned crocodile Aldabrachampsus dilophus Brochu, 2006, the giant tortoise Aldabrachelys cf. gigantea Loveridge & Williams, 1957, an Oplurus iguana and terrestrial skinks (Arnold, 1979). At the younger Point Hodoul fossil deposit, the occurrence of giant tortoise, iguana, skinks and Dryolimnas show that the atoll was seemingly rapidly recolonized on re-emergence, at least from 100 000 YBP (Taylor et al., 1979). The presence of Dryolimnas at both deposits requires explanation. The Bassin Cabri humeri indicate the rail was already flightless at ~127 000+ YBP during the Middle Pleistocene (Fig. 6); therefore, it must have disappeared, along with the other terrestrial fauna, when the atoll was completely submerged (Thomson & Walton, 1972; Taylor et al., 1979). Furthermore, characters of the tarsometatarsus in the Pleistocene specimen suggest that it had evolved a degree of flightlessness at least comparable with D. c. abbotti (Harrison & Walker, 1978), being shorter and more robust than the nominate and D. c. aldabranus (Fig. 7). This, and its presence on Aldabra today, provides irrefutable evidence that Dryolimnas subsequently recolonized Aldabra after inundation and became flightless for a second time. This scenario may seem surprising, but rails are known to be persistent colonizers of isolated islands and can evolve flightlessness rapidly if suitable conditions exist (Olson, 1977). Therefore, it is likely that the dispersal of nominate Dryolimnas from Madagascar to remote Aldabra occurred on multiple occasions, as did giant tortoises (Taylor et al., 1979). The Point Hodoul fossil record shows that the giant tortoise, iguana, a number of lizard taxa and Dryolimnas successfully recolonized the atoll (Hume et al. 2018), but the iguana and most other lizards subsequently perished. Based on the geological record (Braithwaite et al., 1973), this extinction event appears to be unrelated to inundation and may have been the result of introduced black rats Rattus rattus (Linneaus, 1758), which were present on Aldabra in 1890 (Cheke, 2010) but no doubt arrived much earlier. Figure 6. View largeDownload slide Density plots of measurements (mm) of the humerus of Dryolimnas, showing that Pleistocene Dryolimnas cuvieri nestles in with the flightless species. Abbreviations: TL, total length; PW, proximal width; PD, proximal depth; SW, shaft width; SD, shaft depth; DW, distal width; DD, distal depth; (n), number of specimens; (m), mean; SD, Standard Deviation. Figure 6. View largeDownload slide Density plots of measurements (mm) of the humerus of Dryolimnas, showing that Pleistocene Dryolimnas cuvieri nestles in with the flightless species. Abbreviations: TL, total length; PW, proximal width; PD, proximal depth; SW, shaft width; SD, shaft depth; DW, distal width; DD, distal depth; (n), number of specimens; (m), mean; SD, Standard Deviation. Figure 7. View largeDownload slide Density plots of measurements (mm) of the tarsometatarsus of Dryolimnas, showing that Pleistocene Dryolimnas cuvieri approximates flightless species. Abbreviations: DW, distal width; DD, distal depth; TMD, greatest depth taken proximal to trochlea. metatarsi II; (n), number of specimens; (m), mean; SD, Standard Deviation. Figure 7. View largeDownload slide Density plots of measurements (mm) of the tarsometatarsus of Dryolimnas, showing that Pleistocene Dryolimnas cuvieri approximates flightless species. Abbreviations: DW, distal width; DD, distal depth; TMD, greatest depth taken proximal to trochlea. metatarsi II; (n), number of specimens; (m), mean; SD, Standard Deviation. Only relatively few taxa from the Middle to Upper Pleistocene fossil deposits on Aldabra survived into the Holocene. Of those that did, apart from breeding sea birds, the most notable are adept open-water travellers, including giant tortoises (by floating) (Gerlach et al., 2006) and Dryolimnas rails (periodic, long-distance flight dispersal) (Wanless & Hockey, 2008). Evidence of multiple avian colonization events with recurring flightlessness are extremely rare in the fossil record (e.g. Olson & James, 1991; Fulton et al., 2012), especially on smaller oceanic islands where long-term preservation of fossiliferous material is generally poor. We know of no other example in Rallidae, or of birds in general, that demonstrates this phenomenon so evidently. Only on Aldabra, which has the oldest palaeontological record of any oceanic island in the Indian Ocean region (Thomson & Walton, 1972), is fossil evidence available that demonstrates the effects of changing sea levels on extinction and recolonization events. Conditions were such on Aldabra, the most important being the absence of terrestrial predators and competing mammals, that a Dryolimnas rail was able to evolve flightlessness independently on each occasion. ACKNOWLEDGEMENTS We thank Robert Prŷs-Jones, Julia Heinen, Anthony Cheke and an anonymous reviewer for comments that helped improve this paper, and we especially thank Julia Heinen for providing the excellent statistical figures. We thank Storrs Olson, Helen James, Jennifer Strotman and Mark Florence (USNM) for the long-term loan of the John Becker Aldabra material. We thank Sandra Chapman and Lorna Steel (NHMUK) for access to material in their care; Harry Taylor (NHMUK) for photography and Richard Hing (University of Portsmouth) for some fossil preparation. We especially thank the Percy Sladen Centenary Fund whose financial support made this research possible. SUPPORTING INFORMATION Supporting information may be found in the online version of this article at the publisher’s web-site. Table S1. Summary statistics for measurements (mm) of the humerus of Dryolimnas. Table S2. Summary statistics for measurements (mm) of the tarsometatarsus of Dryolimnas. TableS3. Raw measurements (mm) of the humerus of Dryolimnas. Table S4. Raw measurements (mm) of the tarsometatarsus of Dryolimnas. REFERENCES Andreas P , Reijmer JJG , Fürstenau J , Kinkel H , Betzler C . 2012 . Relationship between Late Pleistocene sea-level variations, carbonate platform morphology and aragonite production (Maldives, Indian Ocean) . Sedimentology 59 : 1640 – 1658 . Google Scholar Crossref Search ADS Arnold EN . 1979 . Fossil reptiles from Aldabra Atoll, Indian Ocean . Bulletin of the British Museum (Natural History), Zoology 29 : 85 – 116 . Baumel JJ , Witmer LM . 1993 . Osteologia. In: Baumel JJ , King AS , Breazile JE , Evans HE , Vanden Berge JC , eds. Handbook of avian anatomy: nomina anatomica avium , 2 nd edn. Cambridge : Publications of the Nuttall Ornithological Club , 45 – 132 . Braithwaite CJR . 1984 . Geology of the Seychelles. In: Stoddart DR , ed. Biogeography and ecology of the Seychelles Islands . The Hague : Dr W. Junk Publishers , 17 – 38 . Braithwaite CJR , Taylor JD , Kennedy WJ . 1973 . The evolution of an atoll: the depositional and erosional history of Aldabra . Philosophical Transactions of the Royal Society of London B 266 : 307 – 340 . Google Scholar Crossref Search ADS Brochu CA . 2006 . A new miniature horned crocodile from the Quaternary of Aldabra Atoll, western Indian Ocean . Copeia 2 : 149 – 158 . Google Scholar Crossref Search ADS Cheke A . 2010 . The timing of arrival of humans and their commensal animals on Western Indian Ocean oceanic Islands . Phelsuma 18 : 38 – 69 . Collar NJ . 1993 . The conservation status in 1982 of the Aldabran white-throated rail Dryolimnas cuvieri aldabranus . Bird Conservation International 3 : 299 – 305 . Google Scholar Crossref Search ADS Fulton TL , Letts B , Shapiro B . 2012 . Multiple losses of flight and recent speciation in steamer ducks . Proceedings of the Royal Society B, Biological Sciences 279 : 2339 – 2346 . Google Scholar Crossref Search ADS Gerlach J , Muir C , Richmond MD . 2006 . The first substantiated case of trans-oceanic tortoise dispersal . Journal of Natural History 40 : 2403 – 2408 . Google Scholar Crossref Search ADS Günther A . 1879 . On the occurrence of a land-rail (Rallus) in the Island of Aldabra . Annals and Magazine of Natural History 3 : 164 – 168 . Google Scholar Crossref Search ADS Harrison CJO , Walker CA . 1978 . Pleistocene bird remains from Aldabra Atoll, Indian Ocean . Journal of Natural History 12 : 7 – 14 . Google Scholar Crossref Search ADS Hume JP . 2013 . A synopsis of the pre-human avifauna of the Mascarene Islands. In: Göhlich UB , Kroh A , eds. Proceedings of the 8th international meeting of the Society of avian paleontology and evolution . Vienna : Natural History Museum , 195 – 237 . Hume JP . 2017 . Extinct birds , 2 nd edn. London : Christopher Helm . Hume JP , Martill D , Hing R . 2018 . A palaeontological review of Aldabra Atoll, Aldabra Group, Seychelles . PlosOne . doi: https://doi.org/10.1371/journal.pone.0192675 . Perry CA , Hsu KJ . 2000 . Geophysical, archaeological, and historical evidence support a solar-output model for climate change . PNAS 97 : 12433 – 12438 . Google Scholar Crossref Search ADS PubMed Loveridge A , Williams EE . 1957 . Revision of the African tortoises and turtles of the suborder Cryptodira . Bulletin of the Museum of Comparative Zoology, Harvard 115 : 161 – 557 . Mourer-Chauviré C , Bour R , Ribes S , Moutou F . 1999 . The avifauna of Réunion Island (Mascarene Islands) at the time of the arrival of the first Europeans . Smithsonian Contributions to Paleobiology 89 : 1 – 38 . Nicoll MJ . 1908 . Three voyages of a naturalist . London : Witherby and Co . Olson SL . 1977 . A synopsis of the fossil Rallidae. In: Ripley SD , ed. Rails of the world. A monograph of the family Rallidae . Boston : David R. Godine , 338 – 378 . Olson SL , James HF . 1991 . Descriptions of 32 new species of birds from the Hawaiian Islands: part 1, non-Passeriformes . Ornithological Monographs 45 : 1 – 88 . Google Scholar Crossref Search ADS Pucheran MLD . 1845 . Notes sur quelques espèces Madécasses de l’ordre des Échassiers . Revue Zoologique par la Société Cuvierienne 1845 : 277 – 280 . Ridgway R . 1894 . Descriptions of some new birds from Aldabra, Assumption, and Gloriosa Islands, collected by Dr W. L. Abbott . Proceedings of the United States National Museum 17 : 371 – 373 . Google Scholar Crossref Search ADS Safford R , Hawkins F . 2013 . Birds of Africa, vol. VIII: the Malagasy region . London : Christopher Helm . Stoddart DR , Wright CA . 1967 . Geography and ecology of Aldabra Atoll . Atoll Research Bulletin 118 : 11 – 52 . Taylor JD , Braithwaite CJR , Peake JF , Arnold EN . 1979 . Terrestrial faunas and habitats of Aldabra during the Late Pleistocene . Philosophical Transactions of the Royal Society of London B 286 : 47 – 66 . Google Scholar Crossref Search ADS Thomson J , Walton A . 1972 . Redetermination of chronology of Aldabra Atoll by 230Th/234U dating . Nature 240 : 145 – 146 . Google Scholar Crossref Search ADS Wanless RM , Hockey PAR . 2008 . Natural behaviour of the Aldabra Rail (Dryolimnas [cuvieri] aldabranus) . Wilson Journal of Ornithology 120 : 50 – 61 . Google Scholar Crossref Search ADS © 2019 The Linnean Society of London, Zoological Journal of the Linnean Society This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)

Journal

Zoological Journal of the Linnean SocietyOxford University Press

Published: Jun 25, 2019

References

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create folders to
organize your research

Export folders, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off