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Seeing the forest for the trees—and the grasses: revisiting the evidence for grazer-maintained grasslands in Madagascar's Central Highlands

2021; Royal Society; Volume: 288; Issue: 1950 Linguagem: Inglês

10.1098/rspb.2020.1785

1471-2954

Brooke E. Crowley, Laurie R. Godfrey, James P. Hansford, Karen E. Samonds,

Archaeology and Rock Art Studies

You have accessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Crowley Brooke E., Godfrey Laurie R., Hansford James P. and Samonds Karen E. 2021Seeing the forest for the trees—and the grasses: revisiting the evidence for grazer-maintained grasslands in Madagascar's Central HighlandsProc. R. Soc. B.2882020178520201785http://doi.org/10.1098/rspb.2020.1785SectionSupplemental MaterialYou have accessCommentSeeing the forest for the trees—and the grasses: revisiting the evidence for grazer-maintained grasslands in Madagascar's Central Highlands Brooke E. Crowley Brooke E. Crowley http://orcid.org/0000-0002-8462-6806 Departments of Geology and Anthropology, University of Cincinnati, Cincinnati, OH, USA [email protected] Google Scholar Find this author on PubMed Search for more papers by this author , Laurie R. Godfrey Laurie R. Godfrey http://orcid.org/0000-0001-9997-0207 Department of Anthropology, University of Massachusetts, Amherst, MA, USA Google Scholar Find this author on PubMed Search for more papers by this author , James P. Hansford James P. Hansford http://orcid.org/0000-0002-5702-8915 Institute of Zoology, Zoological Society of London, Regent's Park, London, UK Department of Biological Sciences, Northern Illinois University, DeKalb, IL, USA Google Scholar Find this author on PubMed Search for more papers by this author and Karen E. Samonds Karen E. Samonds http://orcid.org/0000-0003-3597-9215 Department of Biological Sciences, Northern Illinois University, DeKalb, IL, USA Google Scholar Find this author on PubMed Search for more papers by this author Brooke E. Crowley Brooke E. Crowley http://orcid.org/0000-0002-8462-6806 Departments of Geology and Anthropology, University of Cincinnati, Cincinnati, OH, USA [email protected] Google Scholar Find this author on PubMed , Laurie R. Godfrey Laurie R. Godfrey http://orcid.org/0000-0001-9997-0207 Department of Anthropology, University of Massachusetts, Amherst, MA, USA Google Scholar Find this author on PubMed , James P. Hansford James P. Hansford http://orcid.org/0000-0002-5702-8915 Institute of Zoology, Zoological Society of London, Regent's Park, London, UK Department of Biological Sciences, Northern Illinois University, DeKalb, IL, USA Google Scholar Find this author on PubMed and Karen E. Samonds Karen E. Samonds http://orcid.org/0000-0003-3597-9215 Department of Biological Sciences, Northern Illinois University, DeKalb, IL, USA Google Scholar Find this author on PubMed Published:12 May 2021https://doi.org/10.1098/rspb.2020.1785 Review history Seeing the forest for the trees—and the grasses: revisiting the evidence for grazer-maintained grasslands in Madagascar's Central Highlands Today, grasslands cover approximately 80% of Madagascar [1,2], but their extent prior to recent landscape modification remains elusive. Numerous studies converge to suggest that forest cover was much more widespread greater than 1000 years ago and even 100 years ago [3–7]. While researchers initially regarded grasslands as primarily anthropogenic (e.g. [8–10]), the view has been challenged by the diversity and age of endemic grass lineages. This shift in perspective started when Bond et al. [1] suggested that C4 grasses have existed on Madagascar since the late Miocene (e.g. [11]). These inferences were based on (i) C4 grasses, including endemic species, being remarkably diverse in Madagascar, (ii) the species composition of grassy biomes varying geographically (following climate and elevational gradients similar to South Africa), and (iii) grassy biomes including endemic graminoid, herbaceous and woody species. Bond et al. [1] also observed that Malagasy invertebrate and vertebrate groups have grassland specialists. Hackel et al. [12] found support for a Miocene to Pliocene origin of Madagascar's grassy biomes, while Vorontsova et al. [2] demonstrated that roughly 40% of Madagascar's grass species are endemic. There is particularly high diversity and spatial and ecological turnover of endemic grasses in Madagascar's Central Highlands, a region generally considered highly anthropogenically modified and biologically impoverished [4].Solofondranohatra et al. [13] confirmed that endemic grasses in central Madagascar are phylogenetically diverse and found both fire- and grazer-adapted assemblages. They reasoned grassy biomes were maintained by fire and native grazers before humans arrived, and that cattle may have replaced native grazers. They further argued that the importance of grassy biomes has been underappreciated and the Malagasy unnecessarily vilified in the traditional deforestation narrative; efforts to reforest with exotic species are misguided. We agree with these basic arguments. However, two fundamental questions remain unresolved: (i) which now-extinct taxa maintained grazer-adapted grasses? (ii) How extensive were grasslands before human arrival?As Solofondranohatra et al. [13] note, published isotope data for Madagascar's Central Highlands are taxonomically limited (favouring lemurs) and scattered across multiple sources and sites [14–19]. We seek to help rectify this gap by summarizing existing radiocarbon and δ13C data and providing new data for lemurs, hippos and a euplerid carnivoran from the ecoregion (figure 1; electronic supplementary material, table S1). Sample preparation and analysis followed [18]. Raw isotope data were normalized using internal reference materials following [20]. Analytical precision and accuracy were 0.29 and 0.27‰, respectively. We compared δ13Ccollagen values with expected values for pure C3 and mixed C3–C4 consumers. To do this, we assumed that most grasses in Central Madagascar use the C4-photosynthetic pathway, based on species lists for the Central Highlands (e.g. [1]), and a valid assumption for tropical and subtropical sites worldwide. No isotope data exist for grasses from central Madagascar. However, globally, C4 plants have a narrow range of δ13C values (−13.1 ± 1.2‰ [21]). For C3 plants, we used δ13C values for plants from Tsinjoarivo (−24.7 to −32.1‰ [22]), a protected area in the eastern Central Highlands 1300–1675 metres above sea level (m.a.s.l.). After accounting for the isotopic difference between tissue and diet (+5‰ for bone collagen; see [23]), as well as isotopic changes in atmospheric CO2 following the industrial revolution (the Suess effect, −1.2‰; see [23]), animals with pure C3 diets should have collagen δ13CSuess values < −19.7‰ while higher values require a mixed C3–C4 diet. Figure 1. Map of Madagascar showing Central Highland subfossil sites included in this study. Basemap modified from commons.wikimedia.org. (Online version in colour.)Download figureOpen in new tabDownload PowerPointWe explored temporal and spatial trends in the isotope data. We broke data down into two elevational bins: high (greater than 1300 m.a.s.l.) and mid-elevation (800–1300 m.a.s.l.). This cutoff is based on differences in climate (higher elevations have cooler temperatures and receive more precipitation), vegetation (mid-altitude versus montane and sclerophyll forest) and considerably reduced bird and mammal species richness above 1300 m.a.s.l. (e.g. [24,25]). We also broke the data into three temporal bins: greater than 19 000 calendar years before present (cal BP), which encompasses the Last Glacial Maximum (LGM); 19 000–11 700 cal BP, which covers the last deglaciation interval; and less than 11 700 cal BP, which covers the Holocene.At high-elevation sites (Antsirabe, Masinandraina and Tsaramody), there are no δ13C data for animals greater than 19 700 cal BP. However, there were shelducks and sheldgeese (Alopochen and Centrornis) at Antsirabe during and just after the LGM, which supports wetland conditions (figure 2). Just one datum exists for the last deglaciation, a hippo from Tsaramody with a δ13CSuess value suggesting a mixed C3–C4 diet (−15.9‰). More data are available for the Holocene. Hippos (all from Antsirabe) had a narrow isotopic range reflecting pure C3 diets (−26.7 to −26.1‰). However, elephant birds (Aepyornis hildebrandti) had elevated δ13CSuess values both at Antsirabe and Masinandraina (−18.3 to −14.6‰), suggesting a mixed C3–C4 diet. A single extinct Malagasy 'aardvark', Plesiorycteropus, had a δ13CSuess value close to the expected threshold for pure C3 consumption (−19.9‰). Figure 2. Boxplots showing δ13C values for vertebrates during three time intervals at (a) three high-elevation sites (Antsirabe, Masiandraina and Tsaramody) and (b) one mid-elevation site (Ampasambazimba). Stars denote taxa with dates but no δ13C values. (Online version in colour.)Download figureOpen in new tabDownload PowerPointAt mid-elevation Ampasambazimba, water birds (Alopochen) were also present greater than 19 700 cal BP (figure 2). A single Archaeolemur dating to 33 168 ± 3563 cal BP had a δ13CSuess value of −16.7‰, supporting some reliance on C4 resources. However, during the last deglaciation and Holocene, lemurs had δ13CSuess values reflecting pure C3 diets (−25.6 to −20.5‰). The carnivoran Cryptoprocta ferox also consumed C3 resources (−21.1‰), while hippopotamuses had variable δ13CSuess values, with some relying on a mixed diet (−24.2 to −14.7‰).Although these data are still rather limited spatially, temporally and particularly taxonomically, they support the notion that Madagascar's Central Highlands were not densely forested prior to and during the LGM. Available evidence for forest-dependent taxa at sites greater than 1300 m.a.s.l. and the elevated δ13Csuess value for the Archaeolemur at mid-elevation are consistent with relatively open habitat at that time. Isotope data also support continued C4 presence at high elevations after the LGM, and at both mid- and high-elevation sites during the Holocene. However, the abundance of lemur and other arboreal taxa implies significant tree cover from the last deglaciation through much of the Holocene.Isotope and radiocarbon data do not obviate the presence of ancient grasslands in Madagascar. However, they also do not support widespread grasslands in central Madagascar throughout the past 30 000+ years. Instead, the data support a mosaic landscape, with fluctuating dominance of different biomes at different elevations and during different windows of time [5,26]. Factors beyond natural fire and grazing (including temperature, rainfall and anthropogenic fires) have probably contributed to the distribution of grassy biomes over time. Additional data will further elucidate the extent of grassy biomes in Madagascar's Central Highlands and which herbivores maintained grazer-dependent taxa. We look forward to helping solve these remaining unknowns so that appropriate management and conservation decisions can be made.Data accessibilityAll data included in this study are provided in the electronic supplementary material, table S1.Authors' contributionsB.E.C. and L.R.G. designed research; K.E.S., L.R.G. and J.P.H. collected data; B.E.C., L.R.G. and J.P.H. analysed data; B.E.C. wrote the paper; L.R.G., K.E.S. and J.P.H. contributed to the interpretation and the revision of the work.All authors gave final approval for publication and agreed to be held accountable for the work performed therein.Competing interestsWe declare we have no competing interests.FundingThis study was supported by National Science Foundation (grant nos. BCS-1749676 and BCS-1750598).FootnotesThe accompanying reply can be viewed at http://dx.doi.org/10.1098/rspb.2021.0388.Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.5415844.© 2021 The Author(s)Published by the Royal Society. All rights reserved.References1. Bond W, Silander JA, Ranoiavonasy J, Ratsirarson J. 2008The antiquity of Madagascar's grasslands and the rise of C4 grassy biomes. J. Biogeogr. 35, 1743-1758. (doi:10.1111/j.1365-2699.2008.01923.x) Crossref, ISI, Google Scholar2. Vorontsova MSet al.2016Madagascar's grasses and grasslands: anthropogenic or natural?Proc. R. Soc. B 283, 20152262. (doi:10.1098/rspb.2015.2262) Link, ISI, Google Scholar3. Harper GJ, Steininger MK, Tucker CJ, Juhn D, Hawkins F. 2007Fifty years of deforestation and forest fragmentation in Madagascar. Environ. Conserv. 34, 325-333. (doi:10.1017/S0376892907004262) Crossref, ISI, Google Scholar4. 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Hixon S, Douglass K, Godfrey L, Eccles L, Crowley B, Rakotozafy L, Clark G, Haberle S, Anderson A, Wright H and Kennett D (2021) Ecological Consequences of a Millennium of Introduced Dogs on Madagascar, Frontiers in Ecology and Evolution, 10.3389/fevo.2021.689559, 9 This Issue12 May 2021Volume 288Issue 1950 Article InformationDOI:https://doi.org/10.1098/rspb.2020.1785PubMed:33978523Published by:Royal SocietyPrint ISSN:0962-8452Online ISSN:1471-2954History: Manuscript received29/07/2020Manuscript accepted08/12/2020Published online12/05/2021Published in print12/05/2021 License:© 2021 The Author(s)Published by the Royal Society. All rights reserved. Citations and impact KeywordsMadagascarvertebratecarbon isotope valueC4 plantsgrazing Subjectsbiochemistrypalaeontologyecology Large datasets are available through Proceedings B's partnership with Dryad