Paleoclimate, ecoregion size, and degree of isolation explain regional biodiversity differences among terrestrial vertebrates within the Congo Basin
DOI:
https://doi.org/10.26496/bjz.2019.28Keywords:
biodiversity, rainforest, conservation, refuge theory, species accumulation curvesAbstract
One of the most widely recognized patterns in ecology is the increase in species richness from poles to tropics. Literature suggests that the Congolian lowland rainforest does not follow this pattern: the Central Congolian forest (CCLF), south of the Congo River, is thought to harbor fewer vertebrate species and endemics than the Northeastern (NELF) and Northwestern lowland rainforests (NWLF) north of the Congo River. We used data from the Global Biodiversity Information Facility (GBIF) database on terrestrial vertebrates (mammals, birds, and reptiles), to test whether differences in sampling effort caused the irregular biodiversity pattern in this region. Our results show that even though the diversity within the Congolian lowland rainforests remains to be fully mapped, current differences in richness are unlikely to be caused by undersampling alone. We argue that the lower vertebrate richness in the CCLF is due to both its relatively small size and isolated position: Forest cover fluctuated throughout the history of the Congo Basin due to climatic variability, reducing speciation and increasing extinction, while immigration towards the CCLF is limited due to the barrier effect of the Congo River. The implications of these findings are discussed in the context of both fundamental ecology and conservation management.References
Abernethy K.A., Coad L., Taylor G., Lee M.E. & Maisels F. (2013). Extent and ecological consequences of hunting in Central African rainforests in the twenty-first century. Philosophical Transactions of the Royal Society B: Biological Sciences 368: 20120303. https://doi.org/10.1098/rstb.2012.0303
Anthony N.M., Johnson-Bawe M., Jeffery K., Clifford S.L., Abernethy K.A., Tutin C.E., Lahm S.A., White L.J.T., Utley J.F., Wickings E.J. & Bruford M.W. (2007). The role of Pleistocene refugia and rivers in shaping gorilla genetic diversity in central Africa. Proceedings of the National Academy of Sciences 104: 20432–20436. https://doi.org/10.1073/pnas.0704816105
Anthony N.M., Atteke C., Bruford M.W., Dallmeier F., Freedman A., Hardy O., Ibrahim B., Jeffery K.J., Johnson M., Lahm S.A., Lepengue N., Lowenstein J.H., Maisels F., Mboumba J.-F., Mickala P., Morgan K., Ntie S., Smith T.B., Sullivan J.P., Verheyen E. & Gonder M.K. (2015). Evolution and conservation of Central African Biodiversity: priorities for future research and education in the Congo Basin and Gulf of Guinea. Biotropica 47: 6–17. https://doi.org/10.1111/btp.12188
Blom A. (2019a). Central Africa: Northern central part of the Democratic Republic of Congo. WWF. Available from https://www.worldwildlife.org/ecoregions/at0104 [accessed 17 August 2018].
Blom A. (2019b). Africa: Cameroon, Central African Republic, Gabon, and Republic of the Congo. World Wildlife Fund. Available from http://worldwildlife.org/ecoregions/at0126 [accessed 6 March 2019].
Blom A. & Schipper J. (2019). Western Africa: Cameroon, Central African Republic, Gabon, and Republic of the Congo. World Wildlife Fund. Available from https://www.worldwildlife.org/ecoregions/at0124 [accessed 17 August 2018].
Brooks T., Balmford A., Burgess N.D., Fjeldså J., Hansen L.A., Moore J.L., Rahbek C. & Williams P. (2001). Toward a blueprint for conservation in Africa. BioScience 51: 613–624. Available from http://www.bioone.org/doi/full/10.1641/0006-3568%282001%29051%5B0613%3ATABFCI %5D2.0.CO%3B2 [accessed 25 March 2019].
CBD (2011). Strategic plan for Biodiversity 2011–2020 and the Aichi Targets. Convention on Biological Diversity, Québec. Available from https://www.cbd.int/sp/ [accessed 25 March 2019].
Chamberlain S. & Salmon M. (2018). rredlist: IUCN Red List Client. Available from https://cran.r-project.org/web/packages/rredlist/rredlist.pdf [accessed 25 March 2019].
Chamberlain S., Barve V., Mcglinn D., Oldoni D., Geffert L. & Ram K. (2018). rgbif: Interface to the Global “Biodiversity” Information Facility API. Available from https://cran.r-project.org/web/packages/rgbif/rgbif.pdf [accessed 25 March 2019].
Chao A. & Jost L. (2012). Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93: 2533–2547. https://doi.org/10.1890/11-1952.1
Chao A., Chazdon R.L., Colwell R.K. & Shen T.-J. (2005). A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecology Letters 8: 148–159. https://doi.org/10.1111/j.1461-0248.2004.00707.x
Chao A., Chazdon R.L., Colwell R.K. & Shen T.J. (2006). Abundance-based similarity indices and their estimation when there are unseen species in samples. Biometrics 62: 361–371. https://doi.org/10.1111/j.1541-0420.2005.00489.x
Chao A., Gotelli N.J., Hsieh T.C., Sander E.L., Ma K.H., Colwell R.K. & Ellison A.M. (2014). Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs 84: 45–67. https://doi.org/10.1890/13-0133.1
Chao A., Ma K.H. & Hsieh T.C. (2015). SpadeR: Species Prediction and Diversity Estimation with R. Available from https://cran.r-project.org/web/packages/SpadeR/index.html [accessed 25 March 2019].
Chapman C.A.(1983). Speciation of tropical rainforest primates of Africa: insular biogeography. African Journal of Ecology 21: 297–308. https://doi.org/10.1111/j.1365-2028.1983.tb00329.x
Colyn M., Gautier-Hion A. & Verheyen W.(1991). A re-appraisal of palaeoenvironmental history in Central Africa: evidence for a major fluvial refuge in the Zaire Basin. Journal of Biogeography 18: 403–407. https://doi.org/10.2307/2845482
de Klerk H.M., Crowe T.M., Fjeldså J. & Burgess N.D. (2002). Patterns of species richness and narrow endemism of terrestrial bird species in the Afrotropical region. Journal of Zoology 256: 327–342. https://doi.org/10.1017/S0952836902000365
de Klerk H.., Fjeldså J., Blyth S. & Burgess N. (2004). Gaps in the protected area network for threatened Afrotropical birds. Biological Conservation 117: 529–537. https://doi.org/10.1016/j.biocon.2003.09.006
de Menocal P.B. (2004). African climate change and faunal evolution during the Pliocene-Pleistocene. Earth and Planetary Science Letters 220: 3–24. https://doi.org/10.1016/S0012-821X(04)00003-2
Eriksson J., Hohmann G., Boesch C. & Vigilant L. (2004). Rivers influence the population genetic structure of bonobos (Pan paniscus). Molecular Ecology 13: 3425–3435. https://doi.org/10.1111/j.1365-294X.2004.02332.x
ESRI 2008. ArcGIS. Version 9.3. Environmental Systems Research Institute, Inc. Redlands, CA.
Fayolle A., Swaine M.D., Bastin J.-F., Bourland N., Comiskey J.A., Dauby G., Doucet J.-L., Gillet J.-F., Gourlet-Fleury S., Hardy O.J., Kirunda B., Kouamé F.N. & Plumptre A.J. (2014). Patterns of tree species composition across tropical African forests. Journal of Biogeography 41: 2320–2331. https://doi.org/10.1111/jbi.12382
Fine P.V.A. (2015). Ecological and evolutionary drivers of geographic variation in species diversity. Annual Review of Ecology, Evolution and Systematics 46: 369–392. https://doi.org/10.1146/annurev-ecolsys-112414-054102
Fjeldså J. & Lovett J.C. (1997). Geographical patterns of old and young species in African forest biota: The significance of specific montane areas as evolutionary centres. Biodiversity and Conservation 6: 325–346. https://doi.org/10.1023/A:1018356506390
Gambalemoke M., Mukinzi I., Amundala D., Gembu T., Kaswera K., Barrière P., Colyn M., Hutterer R., Kennis J., Leirs H., Vanlinden B. & Verheyen E. (2008). Microgeographical distribution of shrews (Mammalia, Soricidae) in the Congo River basin (Kisangani, DR Congo). Mammalia 72: 213–222. https://doi.org/10.1515/MAMM.2008.043
Gaston K.J. (2000). Global patterns in biodiversity. Nature 405: 220–7. https://doi.org/10.1038/35012228
Gibson L., Lee T.M., Koh L.P., Brook B.W., Gardner T.A., Barlow J., Peres C.A., Bradshaw C.J., Laurance W.F., Lovejoy T.E. & Sodhi N.S. (2011). Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478: 378–81. https://doi.org/10.1038/nature10425
Gotelli N.J. & Colwell R.K. (2001). Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters 4: 379–391. https://doi.org/10.1046/j.1461-0248.2001.00230.x
Graham C.H., Moritz C. & Williams S.E. (2006). Habitat history improves prediction of biodiversity in rainforest fauna. Proceedings of the National Academy of Sciences 103: 632–636. https://doi.org/10.1073/pnas.0505754103
Grytnes J.-A. & McCain C.M. (2007). Elevational trends in biodiversity. In: Levin S.A. (ed.) Encyclopedia of Biodiversity: 1–8. Elsevier.
Hall B.P. & Moreau R.E. (1970). An Atlas of Speciation in African Passerine Birds. Trustees of the British Museum (Natural History), London.
Harcourt A.H. & Wood M.A. (2012). Rivers as barriers to primate distributions in Africa. International Journal of Primatology 33: 168–183. https://doi.org/10.1007/s10764-011-9558-z
Hassanin A., Khouider S., Gembu G.C., Goodman S.M., Kadjo B., Nesi N., Pourrut X., Nakouné E. & Bonillo C. (2015). The comparative phylogeography of fruit bats of the tribe Scotonycterini (Chiroptera, Pteropodidae) reveals cryptic species diversity related to African Pleistocene forest refugia. Comptes Rendus - Biologies 338: 197–211. https://doi.org/10.1016/j.crvi.2014.12.003
Hassanin A., Colombo R., Gembu G.C., Merle M., Tu V.T., Görföl T., Akawa P.M., Csorba G., Kearney T., Monadjem A. & Ing R.K. (2018). Multilocus phylogeny and species delimitation within the genus Glauconycteris (Chiroptera, Vespertilionidae), with the description of a new bat species from the Tshopo Province of the Democratic Republic of the Congo. Journal of Zoological Systematics and Evolutionary Research 56: 1–22. https://doi.org/10.1111/jzs.12176
Hernandez P.A., Graham C.H., Master L.L. & Albert D.L. (2006). The effect of sample size and species characteristics on performance of different species distribution modeling methods. Ecography 29 : 773–785. https://doi.org/10.1111/j.0906-7590.2006.04700.x
Hsieh T.C., Ma K.H. & Chao A. (2016). iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Available from https://cran.r-project.org/web/packages/iNEXT/iNEXT.pdf [accessed 25 March 2019].
Huntley J.W. & Voelker G. (2016). Cryptic diversity in Afro-tropical lowland forests: the systematics and biogeography of the avian genus Bleda. Molecular Phylogenetics and Evolution 99: 297–308. https://doi.org/10.1016/j.ympev.2016.04.002
Hvilsom C., Carlsen F., Heller R., Jaffré N. & Siegismund H.R. (2014). Contrasting demographic histories of the neighboring bonobo and chimpanzee. Primates 55: 101–112. https://doi.org/10.1007/s10329-013-0373-3
IUCN (2018). The IUCN Red List of Threatened Species. Version 2018-2. Available from http://www.iucnredlist.org [accessed 10 January 2019].
Jacquet F., Nicolas V., Colyn M., Kadjo B., Hutterer R., Decher J., Akpatou B., Cruaud C. & Denys C. (2014). Forest refugia and riverine barriers promote diversification in the West African pygmy shrew (Crocidura obscurior complex, Soricomorpha). Zoologica Scripta 43: 131–148. https://doi.org/10.1111/zsc.12039
Jetz W. & Fine P.V.A. (2012). Global gradients in vertebrate diversity predicted by historical area-productivity dynamics and contemporary environment. PLoS Biology 10: e1001292. https://doi.org/10.1371/journal.pbio.1001292
Katuala P.G.B., Kennis J., Nicolas V., Wendelen W., Hulselmans J., Verheyen E., Van Houtte N., Dierckx T., Dudu A.M. & Leirs H. (2008). The presence of Praomys, Lophuromys, and Deomys species (Muridae, Mammalia) in the forest blocks separated by the Congo River and its tributaries (Kisangani region, Democratic Republic of Congo). Mammalia 72: 223–228. https://doi.org/10.1515/MAMM.2008.044
Kennis J., Nicolas V., Hulselmans J., Katuala P.G.B., Wendelen W., Verheyen E., Dudu A.M. & Leirs H. (2011). The impact of the Congo River and its tributaries on the rodent genus Praomys: speciation origin or range expansion limit? Zoological Journal of the Linnean Society 163: 983–1002. https://doi.org/10.1111/j.1096-3642.2011.00733.x
Lewin A., Feldman A., Bauer A.M., Belmaker J., Broadley D.G., Chirio L., Itescu Y., LeBreton M., Maza E., Meirte D., Nagy Z.T., Novosolov M., Roll U., Tallowin O., Trape J.F., Vidan E. & Meiri S. (2016). Patterns of species richness, endemism and environmental gradients of African reptiles. Journal of Biogeography 43: 2380–2390. https://doi.org/10.1111/jbi.12848
Louette M. (1992). Barriers, contact zones and subspeciation in central equatorial Africa. Bulletin B.O.C. Centenary Suppl 112A: 209–216.
Lovett J.C., Rudd S., Taplin J. &, Frimodt-Møller C. (2000). Patterns of plant diversity in Africa south of the Sahara and their implications for conservation management. Biodiversity and Conservation 9: 37–46. https://doi.org/10.1023/A:1008956529695
Maley J. (1996). The African rain forest – main characteristics of changes in vegetation and climate from the Upper Cretaceous to the Quaternary. Proceedings of the Royal Society of Edinburgh, Section B, Biological Sciences 104: 31–73. https://doi.org/10.1017/S0269727000006114
Maley J., Doumenge C., Giresse P., Mahé G., Philippon N., Hubau W., Lokonda M.O., Tshibamba J.M. & Chepstow-Lusty A. (2018). Late Holocene forest contraction and fragmentation in central Africa. Quaternary Research 89: 43–59. https://doi.org/10.1017/qua.2017.97
Myers Thompson J.A. (2003). A model of the biogeographical journey from Proto-pan to Pan paniscus. Primates, Journal of Primatology 44: 191–7. Available from http://europepmc.org/abstract/med/12687485 [accessed 25 March 2019].
Nicolas V., Verheyen E., Verheyen W.N., Hulselmans J., Dillen M., Akpatou B., Dudu A.M., Wendelen W. & Colyn M. (2005). Systematics of African lowland rainforest Praomys (Rodentia, Muridae) based on molecular and craniometrical data. Zoological Journal of the Linnean Society 145: 539–553. https://doi.org/10.1111/j.1096-3642.2005.00196.x
Olayemi A., Nicolas V., Hulselmans J., Missoup A.D., Fichet-Calvet E., Amundala D., Dudu A.M., Dierckx T., Wendelen W., Leirs H. & Verheyen E. (2012). Taxonomy of the African giant pouched rats (Nesomyidae: Cricetomys): molecular and craniometric evidence support an unexpected high species diversity. Zoological Journal of the Linnean Society 165: 700–719. https://doi.org/10.1111/j.1096-3642.2012.00823.x
Olson D.M., Dinerstein E., Wikramanayake E.D., Burgess N.D., Powell G.V.N., Under-wood E.C., D’Amico J.A., Itoua I., Strand H.E., Morrison J.C., Loucks C.J., Allnutt T.F., Ricketts T.H., Kura Y., Lamoreux J.F., Wettengel W.W., Hedao P. & Kassem K.R. (2001). Terrestrial ecoregions of the world: a new map of life on earth. BioScience 51: 933–938. Available from https://bioone.org/journals/BioScience/volume-51/issue-11/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2/Terrestrial-Ecoregions-of-the-World--A-New-Map-of/10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2.full [accessed 25 March 2019].
Parmentier I., Malhi Y., Senterre B., Whittaker R.J., Alonso A., Balinga M.P.B., Bakayoko A., Bongers F., Chatelain C., Comiskey J.A., Cortay R., Djuikouo Kamdem M.N., Doucet J.-L., Gautier L., Hawthorne W.D., Issembe Y.A., Kouamé F.N., Kouka L.A., Leal M.E., Lejoly J., Lewis S.L., Nusbaumer L., Parren M.P.E., Peh K.S.H., Phillips O.L., Sheil D., Sonké B., Sosef M.S.M., Sunderland T.C.H., Stropp J., Ter Steege H., Swaine M.D., Tchouto M.G.P., Van Gemerden B.S., Van Valkenburg J.L.C.H. & Wöll H. (2007). The odd man out? Might climate explain the lower tree alpha-diversity of African rain forests relative to Amazonian rain forests? Journal of Ecology 95: 1058–1071. https://doi.org/10.1111/j.1365-2745.2007.01273.x
Peel M.C., Finlayson B.L. & McMahon T.A. (2007). Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences 11: 1633–1644. https://doi.org/10.5194/hess-11-1633-2007
Phillips H.R.P., Newbold T. & Purvis A. (2017). Land-use effects on local biodiversity in tropical forests vary between continents. Biodiversity and Conservation 26: 2251–2270. https://doi.org/10.1007/s10531-017-1356-2
Plana V. (2004. Mechanisms and tempo of evolution in the African Guineo-Congolian rainforest. Philosophical Transactions of the Royal Society B: Biological Sciences 359: 1585–1594. https://doi.org/10.1098/rstb.2004.1535
R Core Team (2017). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from https://www.R-project.org/ [accessed 25 March 2019].
Reddy S. & Dávalos L.M. (2003). Geographical sampling bias and its implications for conservation priorities in Africa. Journal of Biogeography 30: 1719–1727. https://doi.org/10.1046/j.1365-2699.2003.00946.x
Ricklefs R.E. (2006). Evolutionary diversification and the origin of the relationship of diversity-environment. Ecology 87: 3–13. Available from https://esajournals.onlinelibrary.wiley.com/doi/10.1890/0012-9658%282006%2987% 5B3%3AEDATOO%5D2.0.CO%3B2 [accessed 26 March 2019].
Ricklefs R.E., Schwarzbach A.E. & Renner S.S. (2006). Rate of lineage origin explains the diversity anomaly in the world’s mangrove vegetation. The American Naturalist 168: 805–810. https://doi.org/10.1086/508711
Rowan J., Kamilar J.M., Beaudrot L. & Reed K.E. (2016). Strong influence of palaeoclimate on the structure of modern African mammal communities. Proceedings of the Royal Society B: Biological Sciences 283: 20161207. https://doi.org/10.1098/rspb.2016.1207
Saatchi S.S., Harris N.L., Brown S., Lefsky M., Mitchard E.T.A., Salas W., Zutta B.R., Buermann W., Lewis S.L., Hagen S., Petrova S., White L., Silman M. & Morel A. (2011). Benchmark map of forest carbon stocks in tropical regions across three continents. Proceedings of the National Academy of Sciences of the United States of America 108: 9899–9904. https://doi.org/10.1073/pnas.1019576108
Swenson N.G., Weiser M.D., Mao L., Normand S., Rodríguez M.Á., Lin L., Cao M. & Svenning J.-C. (2016). Constancy in functional space across a species richness anomaly. The American Naturalist 187: E83–E92. https://doi.org/10.1086/685083
Takemoto H., Kawamoto Y. & Furuichi T. (2015). How did bonobos come to range south of the Congo River? Reconsideration of the divergence of Pan paniscus from other Pan populations. Evolutionary Anthropology 24: 170–184. https://doi.org/10.1002/evan.21456
Tosi A.J. (2008). Forest monkeys and Pleistocene refugia: a phylogeographic window onto the disjunct distribution of the Chlorocebus lhoesti species group. Zoological Journal of the Linnean Society 154: 408–418. https://doi.org/10.1111/j.1096-3642.2008.00419.x
Tyukavina A., Hansen M.C., Potapov P., Parker D., Okpa C., Stehman S. V., Kommareddy I. & Turubanova S. (2018). Congo Basin forest loss dominated by increasing smallholder clearing. Science Advances 4: eaat2993. https://doi.org/10.1126/sciadv.aat2993
Willig M.R., Kaufman D.M. & Stevens R.D. (2003). Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annual Review of Ecology, Evolution and Systematics 34: 273–309. https://doi.org/10.1146/annurev.ecolsys.34.012103.144032
World Wildlife Fund (2006). WildFinder: Online Database of Species Distributions. Ver. January 2006. Available from www.worldwildlife.org/WildFinder [accessed 7 January 2019].
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