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Are Madagascar's obligate grazing-lawns ancient and evolved with endemic herbivores, or recently selected by introduced cattle?

2022; Royal Society; Volume: 18; Issue: 9 Linguagem: Inglês

10.1098/rsbl.2022.0212

1744-957X

Grant S. Joseph, Colleen L. Seymour,

Rangeland Management and Livestock Ecology

Open AccessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Joseph Grant S. and Seymour Colleen L. 2022Are Madagascar's obligate grazing-lawns ancient and evolved with endemic herbivores, or recently selected by introduced cattle?Biol. Lett.182022021220220212http://doi.org/10.1098/rsbl.2022.0212SectionSupplemental MaterialOpen AccessCommentAre Madagascar's obligate grazing-lawns ancient and evolved with endemic herbivores, or recently selected by introduced cattle? Grant S. Joseph Grant S. Joseph http://orcid.org/0000-0002-8731-9828 Percy FitzPatrick Institute of African Ornithology, University of Cape Town, Rondebosch 7701, South Africa [email protected] Contribution: Conceptualization, Methodology, Writing – original draft, Writing – review & editing Google Scholar Find this author on PubMed Search for more papers by this author and Colleen L. Seymour Colleen L. Seymour Percy FitzPatrick Institute of African Ornithology, University of Cape Town, Rondebosch 7701, South Africa South African National Biodiversity Institute, Kirstenbosch, Claremont 7735, South Africa Google Scholar Find this author on PubMed Search for more papers by this author Grant S. Joseph Grant S. Joseph http://orcid.org/0000-0002-8731-9828 Percy FitzPatrick Institute of African Ornithology, University of Cape Town, Rondebosch 7701, South Africa [email protected] Contribution: Conceptualization, Methodology, Writing – original draft, Writing – review & editing Google Scholar Find this author on PubMed and Colleen L. Seymour Colleen L. Seymour Percy FitzPatrick Institute of African Ornithology, University of Cape Town, Rondebosch 7701, South Africa South African National Biodiversity Institute, Kirstenbosch, Claremont 7735, South Africa Google Scholar Find this author on PubMed Published:14 September 2022https://doi.org/10.1098/rsbl.2022.0212This article comments on the following:Article CommentaryAssigning shark fin origin using species distribution models needs a reality checkhttps://doi.org/10.1098/rsbl.2020.0907 Vincent Raoult, Michael I. Grant, Ana Paula Barbosa Martins, Leonardo Manir Feitosa, Matias Braccini, Diego Cardeñosa, John Carlson, Andrew Chin, Tobey Curtis, Luís Fernando Carvalho Costa, Luís Fernando Rodrigues Filho, Tommaso Giarrizzo, Jorge Luiz S. Nunes, João Bráullio L. Sales, Jane E. Williamson and Colin A. Simpfendorfer volume 17issue 7Biology Letters14 July 2021 Consensus is growing that Madagascar's largest ecoregion, the Malagasy Central Highlands (MCH), was a habitat mosaic (including forest, woodland, ericoid-scrubland and grasslands) at the period of human settlement of the island [1]. What is less certain is the identity of the grazer purported to have evolved through 'millions of years of grazer and grass coevolution' to form the obligate grazing-lawns found on the MCH [2, p. 8]. Obligate C4-grazing lawns are functionally unique, forming when minimally grazed tall grass swards shift to facultative grazing-lawns (also with tall grasses), before ultimately transforming to short-stature grasses, tolerant of trampling, that spread laterally via rhizomes and stolons [3]. Critical to their formation and maintenance is regular grazing by C4-specialists with high muzzle-width to body-size ratios like African hippopotamus (Hippopotamus amphibius) and wildebeest (Connochaetes taurinus, with ca 95% C4-grass consumption), as opposed to less morphologically adapted, narrow-muzzled mixed-feeders (feeding on a combination of woody, succulent and grass species) like impala (Aepyceros melampus, with only ca 50% C4-grass consumption [3]). Resolution of the debate is central to an emergent functional approach to conservation on this island (a global biodiversity hotspot), that supports processes to facilitate ancient ecological patterns, and avoids practices that do not [1]. Studies of carbon (C) isotopes can yield insights into animal diets, as grazers (consuming C4-grasses) and browsers (consuming C3 woody or crassulacean acid metabalism (CAM) species) have different ratios of 13C isotopes in their bone collagen: pure C4-grazer values exceed −9‰, whereas obligate C3-woody feeders measure below −21.5‰. Hansford & Turvey ([4], p. 1) make a valuable contribution using new analyses of C isotopes, concluding that most Malagasy megafauna fed primarily on C3 and/or CAM, providing evidence of 'widespread browsing ecology'. For specialist grazers, prime candidates have been thought to be the various species of hippopotamus that once inhabited Madagascar [2]. These species are estimated to have gone extinct ca 1200–1050 BP, at the time when agro-pastoralism led to intensive conversion of forest to grassland [5]. Hansford & Turvey's [4] analyses conclude that Malagasy hippopotamus species were predominantly browsers, not grazers. They find that the elephant bird (Aepyornis hildebrandti) obtained up to 48% of its diet from C4-grasses, interpreting this as evidence for a grazing guild among Madagascar's Holocene megaherbivores. Here, we offer an alternative interpretation. With C4-grass representing under half of dietary intake (the remainder being CAM succulent browse and/or C3 material), Aepyornis hildebrandti groups with African mixed-feeding browser guilds (e.g. Aepyceros melampus, Litocranius walleri and Madoqua guentheri) that favour proximity to woodland/scrubland/thicket [6], and not with C4-grazing specialists tolerant of treeless grasslands, that exert the type of top-down control that forms obligate grazing-lawns, like Connochaetes taurinus [3] (figure 1). Figure 1. Suess-corrected δ13C collagen values for Malagasy subfossils, and modern African herbivores (for correction notes and data, see the electronic supplementary material, S1). No Malagasy grazing-guild ate mostly C4-grasses. African mixed-feeders regarded as browsers (e.g. Aepyceros melampus) have higher dietary C4-intake than any Malagasy subfossil species.Download figureOpen in new tabDownload PowerPoint We also offer comment on comparisons with the diet of greater rhea (Rhea americana). Rhea prefer legumes and other dicots, but also eat seeds, fruits, small vertebrates, invertebrates and tall grasses [7,8]. If Aepyornis hildebrandti had similar feeding habits, we would expect bill-feeding in minimally grazed swards that bear no functional similarity to cropped obligate grazing-lawn grasses (indeed, shorter pastoral-grasses negatively impact rhea [8]). Importantly, endemic Malagasy grasses are sensitive to ungulate trampling and grazing, and probably 'evolved under conditions of light grazing or no grazing' ([9], p. 6). Furthermore, Holocene isotope data support 'significant tree cover from the last deglaciation', and 'do not support widespread grasslands in central Madagascar' [10, p. 3]. Domestic cattle, introduced ca 1.5 ka, are the one species in Madagascar that can establish and maintain grazing-lawns [3], and evidence presented here supports MCH obligate grazing-lawns formed through top-down control by these broad-muzzled, C4-specialist grazers. Accepting that treeless grasslands were probably historically far smaller than today [11,12] averts an evolutionary anomaly: the absence of an indigenous C4-specialist grazer that has evolved with treeless grasslands (which today represent Madagascar's largest ecological niche). This, despite the presence of prime candidates, Malagasy hippopotamus species, which Hansford & Turvey [4] affirm were not specialist grazers. Data accessibility The data are provided in the electronic supplementary material [13]. Authors' contributions G.S.J.: conceptualization, methods, writing—original draft, writing—review and editing; C.L.S.: formal analysis, writing—review and editing. Both authors gave final approval for publication and agreed to be held accountable for the work performed therein. Conflict of interest declaration We declare we have no competing interests. Funding We received no funding for this study. FootnotesElectronic supplementary material is available online at rs.figshare.com.The original article can be viewed at http://doi.org/10.1098/rsbl.2020.0907. © 2022 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.References1. Joseph GS, Rakotoarivelo AR, Seymour CL. 2021 How expansive were Malagasy Central Highland forests, ericoids, woodlands and grasslands? A multidisciplinary approach to a conservation conundrum. Biol. Conserv. 261, 109282. (doi:10.1016/j.biocon.2021.109282) Crossref, ISI, Google Scholar2. Solofondranohatra CL, Vorontsova MS, Hempson GP, Hackel J, Cable S, Vololoniaina J, Lehmann CER. 2020 Fire and grazing determined grasslands of central Madagascar represent ancient assemblages. Proc. R. Soc. B 287, 20200598. (doi:10.1098/rspb.2020.0598) Link, ISI, Google Scholar3. Hempson GP et al.. 2015 Ecology of grazing lawns in Africa. Biol. Rev. 90, 979-994. (doi:10.1111/brv.12145) Crossref, PubMed, ISI, Google Scholar4. Hansford JP, Turvey ST. 2022 Dietary isotopes of Madagascar's extinct megafauna reveal holocene browsing and grazing guilds. Biol. Lett. 18, 20220094. (doi:10.1098/rsbl.2022.0094) Link, ISI, Google Scholar5. Hansford JP, Lister AM, Weston EM, Turvey ST. 2021 Simultaneous extinction of Madagascar's megaherbivores correlates with late Holocene human-caused landscape transformation. Quat. Sci. Rev. 263, 106996. (doi:10.1016/j.quascirev.2021.106996) Crossref, ISI, Google Scholar6. Gagnon M, Chew AE. 2000 Dietary preferences in extant African Bovidae. J. Mammal. 81, 490-511. (doi:10.1644/1545-1542(2000)081 2.0.CO;2) Crossref, ISI, Google Scholar7. Martella MB, Navarro JL, Gonnet JM, Mongeildlife SA. 1996 Diet of greater rheas in an agroecosystem of Central Argentina. J. Wildl. Manage. 60, 586-592. (doi:10.2307/3802076) Crossref, ISI, Google Scholar8. Comparatore V, Yagueddú C. 2016 Diet preference and density of the greater rhea (Rhea americana) in grasslands of the flooding Pampa, Argentina. Rev. Bras. Ornitol. 24, 13-20. (doi:10.1007/BF03544323) Crossref, ISI, Google Scholar9. Vorontsova MS et al.. 2016 Madagascar's grasses and grasslands: anthropogenic or natural? Proc. R. Soc. B 283, 20152262. (doi:10.1098/rspb.2015.2262) Link, ISI, Google Scholar10. Crowley BE, Godfrey LR, Hansford JP, Samonds KE. 2021 Seeing the forest for the trees-and the grasses: revisiting the evidence for grazer-maintained grasslands in Madagascar's Central Highlands. Proc. R. Soc. B 288, 20201785. (doi:10.1098/rspb.2020.1785) Link, ISI, Google Scholar11. Joseph GS, Rakotoarivelo AR, Seymour CL. 2022 Tipping points induced by palaeo-human impacts can explain presence of savannah in Malagasy and global systems where forest is expected. Proc. R. Soc. B 289, 20212771. (doi:10.1098/rspb.2021.2771) Link, ISI, Google Scholar12. Joseph GS, Seymour CL. 2021 The unlikely 'antiquity of Madagascar's grasslands': disproportionately forest-limited endemic fauna support anthropogenic transformation from woodland. J. Biogeogr. 48, 2111-2115. (doi:10.1111/jbi.14132) Crossref, ISI, Google Scholar13. Joseph GS, Seymour CL. 2022 Data from: Are Madagascar's obligate grazing-lawns ancient and evolved with endemic herbivores, or recently selected by introduced cattle? Figshare. Google Scholar Previous Article VIEW FULL TEXT DOWNLOAD PDF FiguresRelatedReferencesDetailsCited by Joseph G and Seymour C (2022) Why have Madagascar's mammals, despite being closely‐related to African open‐habitat specialists, failed to radiate into open grasslands?, Journal of Biogeography, 10.1111/jbi.14550, 50:3, (622-627), Online publication date: 1-Mar-2023. Related articlesAssigning shark fin origin using species distribution models needs a reality check14 July 2021Biology Letters This IssueSeptember 2022Volume 18Issue 9 Article InformationDOI:https://doi.org/10.1098/rsbl.2022.0212PubMed:36102011Published by:Royal SocietyOnline ISSN:1744-957XHistory: Manuscript received03/05/2022Manuscript accepted30/08/2022Published online14/09/2022 License:© 2022 The Authors.Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. 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