Genetic data suggest a natural prehuman origin of open habitats in northern Madagascar and question the deforestation narrative in this region - PubMed (original) (raw)
Genetic data suggest a natural prehuman origin of open habitats in northern Madagascar and question the deforestation narrative in this region
Erwan Quéméré et al. Proc Natl Acad Sci U S A. 2012.
Abstract
The impact of climate change and anthropogenic deforestation on biodiversity is of growing concern worldwide. Disentangling how past anthropogenic and natural factors contributed to current biome distribution is thus a crucial issue to understand their complex interactions on wider time scales and to improve predictions and conservation strategies. This is particularly important in biodiversity hotspots, such as Madagascar, dominated by large open habitats whose origins are increasingly debated. Although a dominant narrative argues that Madagascar was originally entirely covered by woodlands, which were destroyed by humans, a number of recent studies have suggested that past climatic fluctuations played a major role in shaping current biome distributions well before humans arrived. Here, we address the question of the origin of open habitats in the Daraina region in northern Madagascar, using a multiproxy approach combining population genetics modeling and remote-sensing analyses. We show that (i) contrary to most regions of Madagascar, the forest cover in Daraina remained remarkably stable over the past 60 y, and (ii) the golden-crowned sifaka (Propithecus tattersalli), a forest-dwelling lemur, underwent a strong population contraction before the arrival of the first humans, hence excluding an anthropogenic cause. Prehuman Holocene droughts may have led to a significant increase of grasslands and a reduction in the species' habitat. This contradicts the prevailing narrative that land cover changes are necessarily anthropogenic in Madagascar but does not preclude the later role played by humans in other regions in which recent lemur bottlenecks have been observed.
Conflict of interest statement
The authors declare no conflict of interest.
Figures
Fig. 1.
Trends in forest cover change in the Daraina region between 1949 and 2002. (A) Circled letters on the satellite imagery of the north of Madagascar indicate the locations of the four places named in the main text and in Fig. 4: Ankarana massif (A), Irodo (B), Vohémar (C), and Andavakoaera (D). (B) Black dots on the map of the Daraina region show the sampling locations of the 105 P. tattersalli social groups genotyped. This figure shows that trends in forest cover change radically in the northwestern (deforestation) and southeastern (forest regeneration) parts of the region as exemplified by the two focus zones [detail (a) and detail (b)] for the periods 1949–1972, 1972–1994, and 1994–2002. The two focus zones are detailed in
Fig. S1
.
Fig. 2.
BF values for the four tested scenarios under the different sampling schemes. H1 corresponds to a contraction attributable to anthropogenic effects following the arrival of Europeans (0–500 Cal. YBP); H2 (500–1,000 Cal. YBP) corresponds to a contraction attributable to anthropogenic effects during the period for which first cities appeared in far northern Madagascar; H3 (1,000–2,000 Cal. YBP) corresponds to the first millennium of human presence, during which human densities were probably very low; and H4 (2,000–10,000 Cal. YBP) corresponds to a contraction caused by environmental factors before the arrival of humans in Madagascar. In the “global sample” analyses (green), samples were taken across the whole sampled area, ignoring any substructure identified in a previous study. In the _K_A (red) and _K_B (blue) analyses, the samples were taken only considering the _K_A and _K_B genetic clusters identified in a previous study (details are provided in Materials and Methods).
Fig. 3.
Most likely period for the start of the population decrease. This figure shows the value of the BF for fixed-length intervals of 500 y between 0 and 50,000 y ago and between 0 and 10,000 y ago (i.e., the Holocene period). The BF measures the weight of evidence for the hypothesis that the population started to decrease in a given interval (Ha) vs. any other time period (Hb). The different solid lines correspond to different sampling strategies described in Materials and Methods: red (genetic unit _K_A), blue (genetic unit _K_B), and green (global sample). BF = 1 indicates that Ha and Hb are equally likely. BF values greater (or smaller) than 1 support Ha (or Hb). We considered BF values >7 as significant evidence for Ha. We indicated, along the time frame, the intervals corresponding to the four tested scenarios (H1–H4) and the historical, palynologicial, and paleontological evidence discussed in the main text.
Similar articles
- Climate change and human colonization triggered habitat loss and fragmentation in Madagascar.
Salmona J, Heller R, Quéméré E, Chikhi L. Salmona J, et al. Mol Ecol. 2017 Oct;26(19):5203-5222. doi: 10.1111/mec.14173. Epub 2017 Jun 28. Mol Ecol. 2017. PMID: 28488335 - Spatial variation in density and total size estimates in fragmented primate populations: the golden-crowned sifaka (Propithecus tattersalli).
Quéméré E, Champeau J, Besolo A, Rasolondraibe E, Rabarivola C, Crouau-Roy B, Chikhi L. Quéméré E, et al. Am J Primatol. 2010 Jan;72(1):72-80. doi: 10.1002/ajp.20754. Am J Primatol. 2010. PMID: 19830745 - The effect of habitat disturbance on the abundance of nocturnal lemur species on the Masoala Peninsula, northeastern Madagascar.
Sawyer RM, Fenosoa ZSE, Andrianarimisa A, Donati G. Sawyer RM, et al. Primates. 2017 Jan;58(1):187-197. doi: 10.1007/s10329-016-0552-0. Epub 2016 Jul 9. Primates. 2017. PMID: 27394434 - Long-term forest-savannah dynamics in the Bolivian Amazon: implications for conservation.
Mayle FE, Langstroth RP, Fisher RA, Meir P. Mayle FE, et al. Philos Trans R Soc Lond B Biol Sci. 2007 Feb 28;362(1478):291-307. doi: 10.1098/rstb.2006.1987. Philos Trans R Soc Lond B Biol Sci. 2007. PMID: 17255037 Free PMC article. Review. - Climate change impacts and vegetation response on the island of Madagascar.
Ingram JC, Dawson TP. Ingram JC, et al. Philos Trans A Math Phys Eng Sci. 2005 Jan 15;363(1826):55-9. doi: 10.1098/rsta.2004.1476. Philos Trans A Math Phys Eng Sci. 2005. PMID: 15598621 Review.
Cited by
- Montane rainforest dynamics under changes in climate and human impact during the past millennia in northern Madagascar.
Montade V, Bremond L, Teixeira H, Kasper T, Daut G, Rouland S, Rasoamanana E, Ramavovolona P, Favier C, Arnaud F, Radespiel U, Behling H. Montade V, et al. R Soc Open Sci. 2024 Aug 21;11(8):230930. doi: 10.1098/rsos.230930. eCollection 2024 Aug. R Soc Open Sci. 2024. PMID: 39169961 Free PMC article. - Remaining forests on the Central Highlands of Madagascar-Endemic and endangered aquatic beetle fauna uncovered.
Ranarilalatiana T, Razafindraleva HA, Granath G, Bukontaite Malm R, Rakotonirina JC, Razafindranaivo V, Ravaomanarivo LHR, Johansson F, Bergsten J. Ranarilalatiana T, et al. Ecol Evol. 2022 Dec 12;12(12):e9580. doi: 10.1002/ece3.9580. eCollection 2022 Dec. Ecol Evol. 2022. PMID: 36523533 Free PMC article. - The importance of well protected forests for the conservation genetics of West African colobine monkeys.
Minhós T, Borges F, Parreira B, Oliveira R, Aleixo-Pais I, Leendertz FH, Wittig R, Fernandes CR, Marques Silva GHL, Duarte M, Bruford MW, Ferreira da Silva MJ, Chikhi L. Minhós T, et al. Am J Primatol. 2023 Jan;85(1):e23453. doi: 10.1002/ajp.23453. Epub 2022 Dec 5. Am J Primatol. 2023. PMID: 36468411 Free PMC article. - How ancient forest fragmentation and riparian connectivity generate high levels of genetic diversity in a microendemic Malagasy tree.
Salmona J, Dresen A, Ranaivoson AE, Manzi S, Le Pors B, Hong-Wa C, Razanatsoa J, Andriaholinirina NV, Rasoloharijaona S, Vavitsara ME, Besnard G. Salmona J, et al. Mol Ecol. 2023 Jan;32(2):299-315. doi: 10.1111/mec.16759. Epub 2022 Nov 23. Mol Ecol. 2023. PMID: 36320175 Free PMC article. - Environmental and anthropogenic influences on movement and foraging in a critically endangered lemur species, Propithecus tattersalli: implications for habitat conservation planning.
Semel MA, Abernathy HN, Semel BP, Cherry MJ, Ratovoson TJC, Moore IT. Semel MA, et al. Mov Ecol. 2022 Apr 15;10(1):20. doi: 10.1186/s40462-022-00320-x. Mov Ecol. 2022. PMID: 35428372 Free PMC article.
References
- Sala OE, et al. Global biodiversity scenarios for the year 2100. Science. 2000;287:1770–1774. - PubMed
- Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GA, Kent J. Biodiversity hotspots for conservation priorities. Nature. 2000;403:853–858. - PubMed
- Ganzhorn JU, Lowry PP, Schatz GE, Sommer S. The biodiversity of Madagascar: One of the world’s hottest hotspots on its way out. Oryx. 2001;35:346–348.
- Laurance W, Peres C. Emerging Threats to Tropical Forests. Chicago: Univ of Chicago Press; 2006.
- IPPC . Climate Change 2007: The Physical Science Basis: Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge Univ Press; 2007.
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources
Miscellaneous