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The role of extinct giant tortoises in the germination of extant baobab Adansonia rubrostipa seeds in Madagascar

Authors:
Seheno Andriantsaralaza at University of Antananarivo
Seheno Andriantsaralaza
Miguel Pedrono at French Agricultural Research Centre for International Development
Miguel Pedrono
Jacques Tassin
Jacques Tassin
Jacques Tassin
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Roger Edmond
Roger Edmond
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Abstract and Figures

Seed passage through the gut of vertebrates is critical for endozoochorous seed dispersal because it may influence seed germination and seed dispersal. Seed retention time in the gut may improve or decrease the seed germination. In Madagascar, extinct giant tortoises were potential seed dispersers of the baobab species. We used the related species Aldabrachelys gigantea, kept in the Tsimbazaza Zoological and Botanical Park (Antananarivo), to test the effect of gut retention time on seed germination in Adansonia rubrostipa. Seed retention time ranged from 15 to 23 days, and almost 87% of defecated seeds remained viable. Germination percentage of defecated seeds did not differ Gut passage (T1) enhanced seed germination percentage compared with that of seeds not extracted from the pulp (T2) but did not differ significantly from pulp removal (T3). The mean retention time (i.e. 17 or 18 days) ensured the most efficient seed dispersal, optimizing the germination rate and allowing a long dispersal distance.
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Note and Record
The role of extinct giant tortoises in the
germination of extant baobab Adansonia
rubrostipa seeds in Madagascar
Seheno Andriantsaralaza
1,2
*, Miguel Pedrono
2,3
, Jacques
Tassin
4
, Edmond Roger
1,2
, Bakolimalala Rakouth
1,2
and
Pascal Danthu
2,4
1
D
epartement de Biologie et Ecologie V
eg
etales, Universit
e
d’Antananarivo, Antananarivo, 101, Madagascar,
2
DP “For^
ets
et Biodiversit
e”, Antananarivo, 101, Madagascar,
3
CIRAD,
UPR AGIRs, Antananarivo, 101, Madagascar and
4
CIRAD,
UPR BSEF, 34398, Montpellier, France
Introduction
Adansonia rubrostipa Jum. & H. Perrier. (Malvaceae) is one of
the six endemic baobab species of Madagascar. The 7–12-cm
diameter fruit has a brown-orange pericarp and a nutritive
pulp around the seeds. Their dispersal agents remain
currently unknown, and these fruits are thus considered
to have no extant dispersal agent species (Wickens & Lowe,
2008). This is a possible consequence of the extinction of
megafauna, including the two species of Madagascan giant
tortoises (Aldabrachelys grandidieri and A. abrupta) (Pedrono
et al., 2013), that may once ensure their seed dispersal
(Guimar~
aes, Galetti & Jordano, 2008).
Retention time of seeds in the digestive tract of the
nearest extant species of giant tortoise, the Aldabran giant
tortoise (Aldabrachelys gigantea), ranges from 7 to 43 days
(Hansen, Kaiser & M€
uller, 2008). Eating of such fruits with
subsequent gut passage and defaecation of intact seeds
may improve germination in a number of mechanistic
ways to: (i) remove fruit pulp, which can inhibit germi-
nation (Samuels & Levey, 2005; Robertson et al., 2006);
(ii) enhance through seeds coat scarification or induce
secondary dormancy (Traveset, 1998); and (iii) transport
seeds away from maternal trees (Blake et al., 2012).
Extinct species of Madagascan giant tortoises were
considered as potentially past seed dispersers of baobabs
(Baum, 1995; Andriantsaralaza et al., 2010). These were
present in Madagascar until 1500–500 years B.P.
(Burleigh & Arnold, 1986). Following other practitioners
(Hansen, Kaiser & M€
uller, 2008; Moolna, 2008), we used
extant Aldabran giant tortoise (Aldabrachelys gigantea) as
ecological analogue for extinct Mascarene giant tortoises
to study the effects of gut passage through giant tortoises
on baobab seed germination.
Materials and methods
Freshly fallen A. rubrostipa fruits were collected in Decem-
ber 2009 near Morondava, western Madagascar. We used
five adult tortoises kept at the Tsimbazaza Zoological and
Botanical Park (Antananarivo), and we offered them
several fruits in March 2010 to determine their appetence.
Then, seeds were collected in faeces each evening. Their
viability was assessed following by Danthu et al. (1995),
which consists on soaking baobab seeds in a solution of
concentrated sulphuric acid (H
2
S0
4
, 95%) during 12 h
before sowing.
Three types of seeds were compared: defecated and
washed seeds (T
1
)
;
seeds extracted from the fruit and sown
with pulp (T
2
); seeds depulped manually and rinsed in
running water (T
3
). Germination trials were carried using
eight replicates for treatment T
1
and five replicates for
treatments T
2
and T
3
.
Germination tests were carried out in the dark at 30°C
on sand moistened. A seed was considered germinated
when the radicle emerged through the seed coat (C^
ome,
1968). Germination test was monitored for 90 days. At the
end of experiment trials, the viability of each ungerminated
seed was assessed by dissection. Mann–Whitney–Wilcoxon
test was used to compare the final germination percentage
and the median germination time (time required for half of
the germinated seeds) between the three treatments.
Results
All of five adult tortoises readily ate most (approximately
3/4) of baobab fruits offered to them. Seed retention times
ranged from 15 to 23 days (Fig. 1).
*Correspondence: E-mail: seheno.andriantsaralaza@cirad.fr
246 ©2013 John Wiley & Sons Ltd, Afr. J. Ecol., 52, 246–249
After acid scarification, the germination percentage of
defecated seeds (44.25 3.78%) did not differ from those
of manually depulped seeds (52 6.06%) (Mann–
Whitney–Wilcoxon: W=4, P=0.34).
Gut passage (T
1
) enhanced seed germination percentage
compared with that of seeds not extracted from the pulp
(T
2
)(W=0, P<0.05) but did not vary significantly from
pulp removal (T
3
)(W=6, P=0.68) (Fig. 2).
Median germination time of defecated seeds (T
1
)
(22 days) was significantly lower than that for depulped
seeds (T
3
) (8 days) (W=0, P<0.05) but was not
significantly different from those of seeds not extracted
from the pulp (T
2
) (34 days) (W=6.5, P=0.45).
Discussion
Giant tortoises ate most of baobab fruits offered to them,
meaning that tortoises have an appetite for these fruits.
Olfactory cues, while poorly understood, may play a role in
fruit selection by tortoises (Liu, Platt & Borg, 2004). The
sweet smell of fruit, indicative of high sugar content, may
have been attractive to giant tortoises.
The percentage germination of defecated seeds scarified
by sulphuric acid means that defecated seeds remained
viable after tortoise gut passage, due to the hardness of
A. rubrostipa seed coat (Razanameharizaka et al., 2006).
Same trends have also been reported by Moolna (2008) on
endemic Mauritian ebony (Diospyros egrettarum) seeds.
Gut passage induced a pulp removal effect which
contains high sugar concentration (Odetokun, 1996) that
may inhibit germination (Samuels & Levey, 2005). How-
ever, mechanical and chemical abrasion by tortoise’s
digestive tract was probably insufficient to release totally
physical dormancy of A. rubrostipa seed and thus improve
germination success. The germination was slower for
defecated seeds than that for depulped seeds. Gut passage
may trigger secondary dormancy following pulp removal
by digestion, although the mechanism involved remains
unclear (Traveset, 1998).
Seed dormancy may play a role in allowing seed
dispersal before the induction of germination, favouring
wider spatial distribution for seedling establishment
(Khurana & Singh, 2001). The African baobab seeds
(A. digitata) remain dormant until 3 years (Danthu et al.,
1995). These are required to release dormancy in
Malvaceae (Baskin & Baskin, 2001). Therefore, secondary
dormancy may likely reduce seedling mortality in
A. rubrostipa in natural conditions.
Considering the long retention time, Madagascan giant
tortoises could have played a predominant role in the
dispersal of baobab seeds to enable them to potentially
colonize new areas. Morphologically, they are similar to
Galapagos giant tortoises (Chelonoidis nigra), which can
disperse seeds more than 4 km from the parent plant
(Blake et al., 2012). Thus, the extinction of Madagascan
giant tortoises and Madagascar’s other megaherbivore,
Fig 1 Cumulative percentage of Adansonia rubrostipa seeds after ingestion by five giant tortoises (Aldabrachelys gigantea). The cumulative
percentage for each day was calculated based on totally defecated seeds after 23 days
©2013 John Wiley & Sons Ltd, Afr. J. Ecol., 52, 246–249
Fate of baobab seeds passed by giant tortoises 247
which were once abundant under the stands of baobab,
can result in poor recruitment in baobab populations (see
Pedrono et al., 2013). Ultimately, this has important
implications for the long-term viability of baobab species
in Madagascar.
Acknowledgements
Financial assistance was received from the French Ministry
of Foreign Affairs (FSP PARRUR project). The authors
thank Jasmin Randrianirina of the PBZT, Antananarivo
and Wilfried Ramahafaly for their assistance.
References
Andriantsaralaza, S., Pedrono, M., Tassin, J., Roger, E. &
Danthu, P. (2010) Baobabs de Madagascar: Un anachronisme
de la dispersion? Bois et For^
ets des Tropiques. 306,7–15.
Baskin, C.C. & Baskin, J.M. (2001) Seeds, Ecology, Biogeography, and
Evolution of Dormancy and Germination. Academic Press, San
Diego.
Baum, D.A. (1995) A systematic revision of Adansonia
(Bombacaceae). Ann. Mo. Bot. Gard. 82, 440–470.
Blake, S., Wikelski, M., Cabrera, F., Guezou, A., Silva, M.,
Sadeghayobi, E., Yackulic, C.B. & Jaramillo, P. (2012) Seed
dispersal by Gal
apagos tortoises. J. Biogeogr. 39, 1961–1972.
Burleigh, R. & Arnold, E.N. (1986) Age and dietary differences of
recently extinct Indian Ocean tortoises (Geochelone s. lat.)
revealed by carbon isotope analysis. Proc. R. Soc. Lond., Ser. B:
Biol. Sci. 227, 137–144.
C^
ome, D. (1968) Probl
emes de terminologie pos
es par la
germination et ses obstacles. Bull. Soc. Franc
ß. Physiol. V
eg 14,
3–9.
Danthu, P., Roussel, J., Gaye, A. & el Mazzoudi, E.H. (1995)
Baobab (Adansonia digitata L.) seed pretreatments for
germination improvement. Seed Sci. Technol. 23, 469–475.
Guimar~
aes, P.R., Galetti, M. & Jordano, P. (2008) Seed dispersal
anachronisms: Rethinking the fruits extinct megafauna ate.
PLoS One 3,1–13.
Hansen, D.M., Kaiser, C.N. & M€
uller, C.B. (2008) Seed dispersal
and establishment of endangered plants on Oceanic Islands: The
Janzen-Connell Model, and the use of ecological analogues. PLoS
One 3,1–13.
Khurana, E. & Singh, J.S. (2001) Ecology of seed and seedling
growth for conservation and restoration of tropical dry forest: a
review. Environ. Conserv. 28,39–52.
Liu, H., Platt, S. & Borg, C. (2004) Seed dispersal by the Florida
box turtle (Terrapene carolina bauri) in pine rockland forests of
the lower Florida Keys, United States. Oecologia 138, 539–546.
Moolna, A. (2008) Preliminary observations indicate that giant
tortoise ingestion improves seed germination for an endemic
ebony species in Mauritius. Afr. J. Ecol. 46, 217–219.
Odetokun, S.M. (1996) The nutritive value of Baobab fruit. Riv Ital
Sostanze Gr.23, 371–373.
Pedrono, M., Griffiths, O.L., Clausen, A., Smith, L.L., Griffiths, C.J.,
Wilm
e, L. & Burney, D.A. (2013) Using a surviving lineage of
Madagascar’s vanished megafauna for ecological restoration.
Biol. Conserv. 159, 501–506.
Fig 2 Cumulative germination success for three treatments: defecated seeds (T
1
); seeds sown with pulp (T
2
) and pulp-removed seeds (T
3
)
©2013 John Wiley & Sons Ltd, Afr. J. Ecol., 52, 246–249
248 Seheno Andriantsaralaza et al.
Razanameharizaka, J., Grouzis, M., Ravelomanana, D. & Danthu, P.
(2006) Seed storage, behaviour and seed germination in African
and Malagasy baobabs (Adansonia species). Seed Sci. Res. 16,
83–88.
Robertson, A.W., Trass, A., Ladley, J.J. & Kelly, D. (2006)
Assessing the benefits of frugivory for seed germination: the
importance of the deinhibition effect. Funct. Ecol. 20,58–66.
Samuels, I.A. & Levey, D.J. (2005) Effects of gut passage on seed
germination: do experiments answer the questions they ask?
Funct. Ecol. 19, 365–368.
Traveset, A. (1998) Effect of seed passage through vertebrate
frugivores’ guts on germination: a review. Perspect. Plant Ecol.
Evol. Syst. 1, 151–190.
Wickens, G. & Lowe, P. (2008) The Baobabs: Pachycauls of Africa,
Madagascar and Australia. Springer, Royal Botanic Gardens,
Kew, UK.
(Manuscript accepted 24 June 2013)
doi: 10.1111/aje.12101
©2013 John Wiley & Sons Ltd, Afr. J. Ecol., 52, 246–249
Fate of baobab seeds passed by giant tortoises 249
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  • Apr 2025
  • Integr Zool
Sundaic giant tortoises ( Manouria emys emys ) are the largest chelonians in Asia. Classified as critically endangered, they are extremely rare throughout their range. The limited knowledge of their behavior and ecology hampers effective conservation initiatives. We integrated GPS tracking, behavioral observations, local ecological knowledge, resource selection functions, spatial distribution modeling, and landscape functional connectivity to assess key aspects of their food habits, movement patterns, and habitat relationships at local and broad scale in Sumatra, Indonesia. Sundaic giant tortoises were predominantly diurnal (93% of activities) and had a mean home range of 27.5 ha (±28.8 SD; N = 3 individuals, autocorrelated kernel density estimate). We identified 40 plant species from 20 families, including ferns, monocots, and dicots, consumed by the tortoises. They consumed the fruits of 30 of these plants, swallowing seeds as large as those of Durio and Artocarpus (>2 × 4 cm), indicating potential seed dispersal over distances exceeding 1 km. Habitat preference analysis at both local and island‐wide scales showed a consistent preference for primary rainforests with steep slopes at moderate altitudes, and near rivers, mostly on the western side of the island. We identified 15 “priority areas,” that is, those with high habitat suitability but lacking formal protection. Among these, only one, Gunung Talang, lacked connectivity with other forest areas, prompting us to propose a wildlife corridor connecting it to Kerinci Seblat National Park. In addition, we argue that Sundaic giant tortoises hold potential for rewilding operations in Sumatra and other parts of their range, emphasizing the need for targeted conservation efforts.
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Ex situ population of Aldabrachelys gigantea (Reptilia: Testudines) in the European Association of Zoos and Aquaria and its perspectives: Hidden extinction and how to prevent it
Article
Full-text available
  • Aug 2023
For the needs of adequate management, we carried out an assessment of the Aldabrachelys gigantea (Schweigger, 1812) population in the institutions of the European Association of Zoos and Aquaria. This population was established a hundred years ago and is continuously growing. Today it is the largest ex situ population of all regional zoo associations. Currently it has 402 individuals, including animals aged over 100 years (up to 162 years). However, our study shows that this increase is depending on the import of individuals from outside sources. The longevity of this species and the relatively low mortality rate in the population makes this process very slow, so that it goes unnoticed. Our predictions show that without imports, this population would become extinct in the long term unless existing natality increases. If there is no change in the reproductive rate (and there is no import), within 20 year the population will drop from current 402 to approx 280 individuals. To maintain current population size 8–9 hatches/year are needed. However, the successful reproduction of A. gigantea in EAZA remains an exceptional event. Our analysis of the demographic and genetic status shows that it has enormous potential. If it was used, the population would have a very long-term perspective secured. Achieving this goal will mean significant improvements in husbandry practices, the issues of which we outline. Rehák I., Velenský P., Zahradníčková V., Martincová I. 2023. Ex situ population of Aldabrachelys gigantea (Reptilia: Testudines) in the European Association of Zoos and Aquaria and its perspectives: Hidden extinction and how to prevent it. Acta Societatis Zoologicae Bohemicae 86: 139-156, 2022 [2023].
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The eco‐evolutionary history of Madagascar presents unique challenges to tropical forest restoration
Article
  • Jun 2022
High biodiversity and endemism combined with persistently high deforestation rates mark Madagascar as one of the hottest biodiversity hot spots. Contemporary rising interest in large-scale reforestation, both globally and throughout Madagascar itself, presents a promising impetus for forest restoration and biodiversity conservation across the island. However, Madagascar may face unique restoration challenges due to its equally unique eco-evolutionary trajectory, which must be understood to enable successful ecological restoration. We conducted a systematic review of potential barriers to restoration for terrestrial forest biomes (rain forests, dry forests, and subhumid highland forests) in Madagascar. Our results indicate that aboveground biomass recovery of Malagasy forests appears to be slower than other tropical forests. We suggest four key synergistic factors that inhibit restoration in Madagascar: (a) lack of resilience to shifting nutrient and fire regimes arising from widespread high-intensity shifting cultivation; (b) predominance of nutrient-poor, highly weathered ferralitic soils; (c) vulnerability of regenerating native trees to competition with invasive species due to their evolutionary isolation; and (d) low seed dispersal into regenerating forests due to the unique dependence of Malagasy trees on dispersal by forest-dependent endangered or extinct primates. However, we note that rigorous experimental study of regenerating forests in Madagascar is currently lacking. There are great opportunity and need for such research to disentangle drivers and interactions inhibiting forest restoration. These studies would enable reforestation practitioners to effectively capitalize on current global momentum to implement the large-scale restoration necessary for the conservation of Madagascar's numerous endemic species. Abstract in Malagasy is available with online material.
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A Systematic Revision of Adansonia (Bombacaceae)
Article
Full-text available
  • Jan 1995
The baobabs (Bombacaceae: Adansonia) are tropical trees native to Africa, Australia, and Madagascar but dispersed widely by humans. The members of the genus are united by several derived characters that serve to distinguish them from other Bombacaceae, including a characteristic, indehiscent fruit with reniform seeds and a powdery pulp. The systematics of Adansonia is revised, with three sections and eight species being recognized. The support for each species is discussed in the context of the "Genealogical Species Concept." Several nomenclatural problems are resolved, and a new combination, A. gibbosa (A. Cunn.) Guymer ex D. Baum, is made. In addition, the ecology, ethnobotany, and conservation status of Adansonia is summarized, focusing especially on the poorly known Malagasy and Australian species.
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Baobabs de Madagascar : un anachronisme de la dispersion ?
Article
Full-text available
  • Dec 2010
La dispersion des semences de baobabs malgaches, Adansonia spp., semble ne jamais avoir été étudiée de manière formelle, à ce jour. Elle relève d’hypothèses que cette synthèse bibliographique a pour objet de réunir. Si l’homme semble jouer un rôle important dans la dispersion d’Adansonia digitata en Afrique, une telle hypothèse reste rarement évoquée à l’égard des espèces malgaches. Divers auteurs privilégient l’hypothèse d’une dispersion anachronique, liée à la disparition de la mégafaune malgache ; mais d’autres évoquent le rôle possible de vertébrés introduits. L’intervention de l’oiseauéléphant, Aepyornis spp., des tortues géantes, Aldabrachelys spp., et des grands lémuriens disparus, Archaeolemur spp., ou actuels est plus particulièrement évoquée, en vis-à-vis du rôle possible d’animaux introduits, zébus, Bos indicus, potamochères, Potamochoerus larvatus. Des expérimentations conduites ex situ sur des animaux indigènes ou introduits, dont certains se rapprochent par leur morphologie ou leur phylogenèse de vertébrés éteints, pourraient éclaircir cette énigme de la dispersion chez les baobabs de Madagascar.
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Using a surviving lineage of Madagascar's vanished megafauna for ecological restoration
Article
Full-text available
  • Mar 2013
  • BIOL CONSERV
a b s t r a c t The extinctions of keystone megafauna during the Pleistocene and Holocene continue to affect extant species and ecosystems. This is particularly acute in southern and western Madagascar where two now extinct species of giant tortoises were once amongst the most dominant herbivores. The extinct giant tortoises are likely to have influenced ecosystem processes by being effective dispersers of large seeds, keeping the understorey open, cycling nutrients, and indirectly regulating fire regimes. As a result of their extinction, ecological interactions and ecosystems have been altered. Given that there is evidence that the extant Aldabran giant tortoise, Aldabrachelys gigantea, is closely related to at least one of these Madagascan giant tortoises, Aldabrachelys abrupta, we propose using captive Aldabran giant tortoises to restore missing ecological functions. This ambitious approach will represent the first continental island restoration project with a surviving lineage of now extinct, endemic megafauna. Translocation of this megafauna species could be a pragmatic and cost-effective tool to contribute to halting the ongoing extinction processes in parts of western and southern Madagascar, and would further understanding of the role of these species in pre-human Madagascan ecosystems.
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Effect of seed passage through vertebrate frugivores' guts on germination: A review
Article
Full-text available
  • Dec 1998
  • PERSPECT PLANT ECOL
The capacity of seeds to germinate after ingestion by frugivores is important for the population dynamics of some plant species and significant for the evolution of plant-frugivore interactions. In this paper the effects of different vertebrates on seed germination of nearly 200 plant species are reviewed, searching for patterns that predict the circumstances in which germination of seeds is enhanced, inhibited, or unaffected by the passage through the digestive tract of a seed disperser. It was found that seed dispersers commonly have an effect on the germinability of seeds, or on the rate of germination, or both, in about 50% of the plants they consume, although the diversity of animal species tested so far is still rather low (42 bird species, 28 non-flying mammals, 10–15 bats, 12 reptiles, 2 fishes). Enhancement of germination occurred about twice as often as inhibition.
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Seed Ecology, Biogeography, and Evolution of Dormancy and Germination
Book
  • Mar 2014
The new edition of Seeds contains new information on many topics discussed in the first edition, such as fruit/seed heteromorphism, breaking of physical dormancy and effects of inbreeding depression on germination. New topics have been added to each chapter, including dichotomous keys to types of seeds and kinds of dormancy; a hierarchical dormancy classification system; role of seed banks in restoration of plant communities; and seed germination in relation to parental effects, pollen competition, local adaption, climate change and karrikinolide in smoke from burning plants. The database for the world biogeography of seed dormancy has been expanded from 3,580 to about 13,600 species. New insights are presented on seed dormancy and germination ecology of species with specialized life cycles or habitat requirements such as orchids, parasitic, aquatics and halophytes. Information from various fields of science has been combined with seed dormancy data to increase our understanding of the evolutionary/phylogenetic origins and relationships of the various kinds of seed dormancy (and nondormancy) and the conditions under which each may have evolved. This comprehensive synthesis of information on the ecology, biogeography and evolution of seeds provides a thorough overview of whole-seed biology that will facilitate and help focus research efforts.
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The Baobabs: Pachycauls of Africa, Madagascar and Australia
Book
  • Jan 2007
First and only fully comprehensive account of all eight species of Adansonia Contains much new information Highly interesting for scientists, academics and laypeople This is the only comprehensive account of all eight species in the genus Adansonia. It describes the historical background from the late Roman period to the present. It covers the extraordinary variety of economic uses of baobabs, famous trees, folk traditions and mythology, art associations, life cycle, natural history, cultivation, conservation, distribution and ecology, and phytogeography. There are also appendices on vernacular names, gazetteer, economics, nutrition and forest mensuration. This book fills a gap in the botanical literature. It deals with a genus that has fascinated and intrigued scientists and lay persons for centuries. It will appeal to scientists and academics as well as tropical horticulturalists, conservationists and general interest readers. It includes all the available scientific information about each of the eight species, and contains a good deal of original research on the history, ethnobotany and biology of the genus. There is even a chapter devoted to areas where further research is required. © 2008 Springer Science + Business Media, B.V. All rights reserved.
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Age and Dietary Differences of Recently Extinct Indian Ocean Tortoises (Geochelone s. lat.) Revealed by Carbon Isotope Analysis
Article
  • Feb 1986
All but one of the seven or eight species of giant tortoise (Geochelone) in the southwest Indian Ocean became extinct by the mid-nineteenth century, leaving many aspects of their history and biology unknown. Radiocarbon dating of fossil remains indicates that the population of G. gigantea on the small island of Assumption was a natural one, predating European activity in the area. It also confirms that the two species known from Mauritius, G. inepta and G. triserrata, were indeed synchronous and that this was also true of the pair found on Madagascar, G. grandidieri and G. abrupta. Survival of both the latter species well into the first millennium A.D. is demonstrated, suggesting that they were still present when the first human colonists arrived and were perhaps exterminated by them. Stable carbon isotope ratios indicate that, apparently unlike other Indian Ocean giant tortoises, G. grandidieri ate a high proportion of plants with C4 metabolism. This may have reduced potential competition with the sympatric G. abrupta.
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