Abstract
To inform regional conservation planning, we assessed mammalian and avian biodiversity in the Djéké Triangle, which is an intact forest with long-term research and tourism focused on western lowland gorillas (Gorilla gorilla gorilla). This critical region serves as a conservation conduit between the Nouabalé-Ndoki National Park (NNNP) in the Republic of Congo and the Dzanga-Ndoki National Park in Central African Republic. Wildlife inventories were conducted to determine if biodiversity in the Djéké Triangle (initially part of a logging concession) was equivalent to the NNNP. Camera traps (CTs) were deployed to estimate species richness, relative abundance, naïve occupancy, and activity patterns of medium-to-large species in mixed species and monodominant Gilbertiodendron forests that comprise the majority of regional terra firma. Species inventories were collected from CTs positioned on a grid and at termite nests throughout the Djéké Triangle and compared to CTs placed in the Goualougo Triangle located within the NNNP. From 10,534 camera days at 65 locations, we identified 34 mammal and 16 bird species. Allaying concerns of wildlife depletion, metrics of species richness in the Djéké Triangle surpassed those of the Goualougo Triangle. Many species were observed to occur across habitats, while others showed habitat specificity, with termite mounds indicated as an important microhabitat feature. Our comparisons of animal activity budgets in different habitat types provide important reference information for other populations and contexts. In conclusion, this study provided empirical evidence of the high conservation value of this region that contributed to increasing the protected status of the Djéké Triangle.
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A Visual Reference Guide for Identifying Birds and Mammals in Camara Traps is provided in the Supplemental Material S1.
References
Abernethy KA, Coad L, Taylor G, Lee ME, Maisels F (2013) Extent and ecological consequences of hunting in Central African rainforests in the twenty-first century. Philos Trans R Soc B 368(1625):20120303.
Agha M, Batter T, Bolas EC, Collins AC, Gomes da Rocha D, Monteza-Moreno CM, Preckler-Quisquater S, Sollmann R (2018) A review of wildlife camera trapping trends across Africa. Afr J Ecol 56(4):694–701
Barlow J, Lennox GD, Ferreira J, Berenguer E, Lees AC, Mac Nally R, Thomson JR, Ferraz SFD, Louzada J, Oliveira VHF, Parry L, Solar RRD, Vieira ICG, Aragao L, Begotti RA, Braga RF, Cardoso TM, de Oliveira RC, Souza CM, Moura NG, Nunes SS, Siqueira JV, Pardini R, Silveira JM, Vaz-de-Mello FZ, Veiga RCS, Venturieri A, Gardner TA (2016) Anthropogenic disturbance in tropical forests can double biodiversity loss from deforestation. Nature 535(7610):144-+
Benítez-López A, Santini L, Schipper AM, Busana M, Huijbregts MAJ (2019) Intact but empty forests? Patterns of hunting-induced mammal defaunation in the tropics. PLoS Biol 17(5):e3000247
Bennett EL, Blencowe E, Brandon K, Brown D, Burn RW, Cowlishaw G, Davies G, Dublin H, Fa JE, Milner-Gulland EJ, Robinson JG, Rowcliffe JM, Underwood FM, Wilkie DS (2007) Hunting for consensus: Reconciling bushmeat harvest, conservation, and development policy in west and central Africa. Conserv Biol 21(3):884–887
Bermejo M, Rodriguez-Teijeiro JD, Illera G, Barroso A, Vila C, Walsh PD (2006) Ebola outbreak killed 5000 gorillas. Science 314(5805):1564–1564
Bessone M, Kühl HS, Hohmann G, Herbinger I, N’Goran KP, Asanzi P, Da Costa PB, Dérozier V, Fotsing EDB, Beka BI, Iyomi MD, Iyatshi IB, Kafando P, Kambere MA, Moundzoho DB, Wanzalire MLK, Fruth B (2020) Drawn out of the shadows: surveying secretive forest species with camera trap distance sampling. J Appl Ecol 57(5):963–974
Billerman SM, Keeney BK, Rodewald PG, Schulenberg TS (2022) Birds of the World. Cornell Laboratory of Ornithology, Ithaca
Blake S, Fay JM (1997) Seed production by Gilbertiodendron dewevrei in the Nouabalé-Ndoki National Park, Congo, and its implications for large mammals. J Trop Ecol 14:885–891
Bohmann K, Evans A, Gilbert MT, Carvalho GR, Creer S, Knapp M, Yu DW, de Bruyn M (2014) Environmental DNA for wildlife biology and biodiversity monitoring. Trends Ecol Evol 29(6):358–367
Boogert NJ, Paterson DM, Laland KN (2006) The implications of niche construction and ecosystem engineering for conservation biology. Bioscience 56:570
Bourlière F (1985) Primate communities - their structure and role in the tropical ecosystems. Int J Primatol 6(1):1–26
Bowkett A, Pegg N, Rovero F, Plowman A (2006) How do you monitor rare and elusive mammals? Counting duikers in Kenya, Tanzania and Zimbabwe. In: Zgrabczyñska ĆPE, Ziomek J (eds) Animals, zoos and conservation. Zoological Garden in Poznan, Poland, pp 21–28
Brakes P, Carroll EL, Dall SRX, Keith SA, McGregor PK, Mesnick SL, Noad MJ, Rendell L, Robbins MM, Rutz C, Thornton A, Whiten A, Whiting MJ, Aplin LM, Bearhop S, Ciucci P, Fishlock V, Ford JKB, Notarbartolo di Sciara G, Simmonds MP, Spina F, Wade PR, Whitehead H, Williams J, Garland EC (2021) A deepening understanding of animal culture suggests lessons for conservation. Proc R Society B 288(1949):20202718
Brncic T, Maisels F, Strindberg S (2018) Results of the 2016–2017 large mammal survey of the Ndoki-Likouala landscape. New York Wildlife Conservation Society, New York
Bruce T, Kamta R, Tabue Mbobda RB, Talla Kanto S, Djibrilla D, Moses I, Deblauwe V, Njabo K, LeBreton M, Ndjassi C, Barichievy C, Olson D (2018) Locating giant ground pangolins (Smutsia gigantea) using camera traps on burrows in the Dja Biosphere reserve, Cameroon. Trop Conserv Sci 11:1940082917749224
Cappelle N, Howe EJ, Boesch C, Kühl HS (2021) Estimating animal abundance and effort–precision relationship with camera trap distance sampling. Ecosphere 12(1):e03299
Caro T, Engilis A, Fitzherbert E, Gardner T (2004) Preliminary assessment of the flagship species concept at a small scale. Anim Conserv 7(1):63–70
Carvalho S, Wessling EG, Abwe EE, Almeida-Warren K, Arandjelovic M, Boesch C, Danquah E, Diallo MS, Hobaiter C, Hockings K, Humle T, Ikemeh RA, Kalan AK, Luncz L, Ohashi G, Pascual-Garrido A, Piel A, Samuni L, Soiret S, Sanz C, Koops K (2022) Using nonhuman culture in conservation requires careful and concerted action. Conserv Lett 15(2):e12860
Cawthorn D-M, Hoffman LC (2015) The bushmeat and food security nexus: a global account of the contributions, conundrums and ethical collisions. Food Res Int 76:906–925
Choosai C, Mathieu J, Hanboonsong Y, Jouquet P (2009) Termite mounds and dykes are biodiversity refuges in paddy fields in North-Eastern Thailand. Environ Conserv 36(1):71–79
Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166
Danielsen F, Burgess ND, Jensen PM, Pirhofer-Walzl K (2010) Environmental monitoring: the scale and speed of implementation varies according to the degree of peoples involvement. J Appl Ecol 47(6):1166–1168
DeFries R, Karanth KK, Pareeth S (2010) Interactions between protected areas and their surroundings in human-dominated tropical landscapes. Biol Cons 143(12):2870–2880
Dupain J, Nackoney J, Mario Vargas J, Johnson PJ, Farfan MA, Bofaso M, Fa JE (2012) Bushmeat characteristics vary with catchment conditions in a Congo market. Biol Cons 146(1):32–40
Effiom EO, Nuñez-Iturri G, Smith HG, Ottosson U, Olsson O (2013) Bushmeat hunting changes regeneration of African rainforests. Proc R Soc B 280(1759):20130246
Elkan P (2003) Ecology and conservation of bongo antelope (Tragelaphus eurycerus) in Lowland Forest, northern Republic of Congo. (Unpublished Ph.D. thesis), University of Minnesota
Elkan P, Parnell R, Smith D (2009) A die-off of large ungulates following a Stomoxys biting fly out-break in lowland forest, northern Republic of Congo. Afr J Ecol 47(4):528–536
Fa JE, Brown D (2009) Impacts of hunting on mammals in African tropical moist forests: a review and synthesis. Mammal Rev 39(4):231–264
Fa JE, Currie D, Meeuwig J (2003) Bushmeat and food security in the Congo Basin: linkages between wildlife and people’s future. Environ Conserv 30(1):71–78
Fa JE, Johnson PJ, Dupain J, Lapuente J, Koster P, Macdonald DW (2004) Sampling effort and dynamics of bushmeat markets. Anim Conserv 7:409–416
Fa JE, Olivero J, Real R, Farfan MA, Marquez AL, Vargas JM, Ziegler S, Wegmann M, Brown D, Margetts B, Nasi R (2015) Disentangling the relative effects of bushmeat availability on human nutrition in central Africa. Sci Rep. https://doi.org/10.1038/srep08168
Fontyen D (2022) Distribution and determinants of mammal assemblages across central African forests PhD Thesis, Liege University
Fonteyn D, Vermeulen C, Deflandre N, Cornelis D, Lhoest S, Houngbégnon FGA, Doucet JL, Fayolle A (2021) Wildlife trail or systematic? Camera trap placement has little effect on estimates of mammal diversity in a tropical forest in Gabon. Remote Sens Ecol Conserv 7(2):321–336
Fragoso JMV, Levi T, Oliveira LFB, Luzar JB, Overman H, Read JM, Silvius KM (2016) Line transect surveys underdetect terrestrial mammals: Implications for the sustainability of subsistence hunting. PLOS ONE 11(4):e0152659
Gardner TA, Barlow J, Sodhi NS, Peres CA (2010) A multi-region assessment of tropical forest biodiversity in a human-modified world. Biol Cons 143(10):2293–2300
Gautier-Hion A, Brugiere D (2005) Significance of riparian forests for the conservation of Central African primates. Int J Primatol 26(3):515–523
Getz WM, Fortmann L, Cumming D, du Toit J, Hilty J, Martin R, Murphree M, Owen-Smith N, Starfield AM, Westphal MI (1999) Sustaining natural and human capital: villagers and scientists. Science 283(5409):1855–1856
Gibson L, Lee TM, Koh LP, Brook BW, Gardner TA, Barlow J, Peres CA, Bradshaw CJA, Laurance WF, Lovejoy TE, Sodhi NS (2011) Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478(7369):378
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4(4):379–391
Grantham HS, Shapiro A, Bonfils D, Gond V, Goldman E, Maisels F, Plumptre AJ, Rayden T, Robinson JG, Strindberg S, Stokes E, Tulloch A, Watson JEM, Williams L, Rickenbach O (2020) Spatial priorities for conserving the most intact biodiverse forests within Central Africa. Environ Res Lett 15(9). https://doi.org/10.1088/1748-9326/ab9fae
Hall J, Harris D, Saltonstall K, Medjibe V, Ashton M, Turner B (2019) Resource acquisition strategies facilitate Gilbertiodendron dewevrei monodominance in African lowland forests. J Ecol 108:433–448
Hansen AJ, Burns P, Ervin J, Goetz SJ, Hansen M, Venter O, Watson JEM, Jantz PA, Virnig ALS, Barnett K, Pillay R, Atkinson S, Supples C, Rodríguez-Buritica S, Armenteras D (2020) A policy-driven framework for conserving the best of earth’s remaining moist tropical forests. Nat Ecol Evolut 4(10):1377–1384
Harris DJ (2002) The vascular plants of the Dzanga-Sangha reserve. National Botanic Garden, Belgium
Hart TB (1990) Monospecific dominance in tropical rain forests. Trends Ecol Evol 5(1):6–11
Hart TB (2001) Forest dynamics in the Ituri Basin (DR Congo). In: White LJT, Weber W, Vedder A, Naughton-Treves I (eds) African rain forest ecology and conservation. Yale University Press, New Heaven, pp 154–164
Hedwig D, Kienast I, Bonnet M, Curran BK, Courage A, Boesch C, Kuehl HS, King T (2018) A camera trap assessment of the forest mammal community within the transitional savannah-forest mosaic of the Bateke Plateau National park, Gabon. Afr J Ecol 56(4):777–790
Hempson GP, Archibald S, Bond WJ (2015) A continent-wide assessment of the form and intensity of large mammal herbivory in Africa. Science 350(6264):1056–1061
Houngbégnon FGA, Cornelis D, Vermeulen C, Sonké B, Ntie S, Fayolle A (2020) Daily Activity Patterns and Co-Occurrence of Duikers Revealed by an Intensive Camera Trap Survey across Central African Rainforests. Animals 10(12)
Howe EJ, Buckland ST, Despres-Einspenner ML, Kuhl HS (2017) Distance sampling with camera traps. Methods Ecol Evol 8(11):1558–1565
IUCN (2022) The IUCN Red List of Threatened Species. Version 2022–1. Retrieved September 19, 2022
Kéry M, Royle JA (2008) Hierarchical Bayes estimation of species richness and occupancy in spatially replicated surveys. J Appl Ecol 45(2):589–598
Khwaja H, Buchan C, Wearn OR, Bahaa-el-din L, Bantlin D, Bernard H, Bitariho R, Bohm T, Borah J, Brodie J, Chutipong W, du Preez B, Ebang-Mbele A, Edwards S, Fairet E, Frechette JL, Garside A, Gibson L, Giordano A, Gopi GV, Granados A, Gubbi S, Harich F, Haurez B, Havmoller RW, Helmy O, Isbell LA, Jenks K, Kalle R, Kamjing A, Khamcha D, Kiebou-Opepa C, Kinnaird M, Kruger C, Laudisoit A, Lynam A, Macdonald SE, Mathai J, Sienne JM, Meier A, Mills D, Mohd-Azlan J, Nakashima Y, Nash HC, Ngoprasert D, Nguyen A, O'Brien T, Olson D, Orbell C, Poulsen J, Ramesh T, Reeder D, Reyna R, Rich LN, Rode-Margono J, Rovero F, Sheil D, Shirley MH, Stratford K, Sukumal N, Suwanrat S, Tantipisanuh N, Tilker A, Van Berkel T, Van der Weyde LK, Varney M, Weise F, Wiesel I, Wilting A, Wong ST, Waterman C, Challender DWS (2019) Pangolins in global camera trap data: Implications for ecological monitoring. Global Ecology and Conservation 20:e00769
Kingdon J (2015) The Kingdon field guide to African mammals, 2nd edn. Princeton University Press, Princeton
Koopmans M, Stokes EJ, Opepa CK, Mouele AM, Abea G, Strindberg S (2021) Wild bongo density estimation and population viability analysis improves conservation management. Global Ecol Conserv 28:e01661
Kuehl HS, Boesch C, Kulik L, Haas F, Arandjelovic M, Dieguez P, Bocksberger G, McElreath MB, Agbor A, Angedakin S, Ayimisin EA, Bailey E, Barubiyo D, Bessone M, Brazzola G, Chancellor R, Cohen H, Coupland C, Danquah E, Deschner T, Dowd D, Dunn A, Egbe VE, Eshuis H, Goedmakers A, Granjon AC, Head J, Hedwig D, Hermans V, Imong I, Jeffery KJ, Jones S, Junker J, Kadam P, Kambere M, Kambi M, Kienast I, Kujirakwinja D, Langergraber KE, Lapuente J, Larson B, Lee K, Leinert V, Llana M, Maretti G, Marrocoli S, Martin R, Mbi TJ, Meier AC, Morgan B, Morgan D, Mulindahabi F, Murai M, Neil E, Niyigaba P, Ormsby LJ, Orume R, Pacheco L, Piel A, Preece J, Regnaut S, Rundus A, Sanz C, van Schijndel J, Sommer V, Stewart F, Tagg N, Vendras E, Vergnes V, Welsh A, Wessling EG, Willie J, Wittig RM, Yuh YG, Yurkiw K, Zuberbuhler K, Kalan AK (2019) Human impact erodes chimpanzee behavioral diversity. Science 363(6434):1453–1458
Leader-Williams N, Dublin HT (2000) Charismatic megafauna as ‘flagship species.’ In: Entwistle A, Dunstone N (eds) Priorities for the conservation of mammalian diversity. Has the panda had its day? Cambridge University Press, Cambridge, pp 53–81
Leclere D, Obersteiner M, Barrett M, Butchart SHM, Chaudhary A, De Palma A, DeClerck FAJ, Di Marco M, Doelman JC, Durauer M, Freeman R, Harfoot M, Hasegawa T, Hellweg S, Hilbers JP, Hill SLL, Humpenoder F, Jennings N, Krisztin T, Mace GM, Ohashi H, Popp A, Purvis A, Schipper AM, Tabeau A, Valin H, van Meijl H, Van Zeist WJ, Visconti P, Alkemade R, Almond R, Bunting G, Burgess ND, Cornell SE, Di Fulvio F, Ferrier S, Fritz S, Fujimori S, Grooten M, Harwood T, Havlik P, Herrero M, Hoskins AJ, Jung M, Kram T, Lotze-Campen H, Matsui T, Meyer C, Nel D, Newbold T, Schmidt-Traub G, Stehfest E, Strassburg BBN, van Vuuren DP, Ware C, Watson JEM, Wu WC, Young L (2020) Bending the curve of terrestrial biodiversity needs an integrated strategy. Nature 585(7826):551
Lindenmayer DB, Margules CR, Botkin DB (2000) Indicators of biodiversity for ecologically sustainable forest management. Conserv Biol 14(4):941–950
Loh J, Green RE, Ricketts T, Lamoreux J, Jenkins M, Kapos V, Randers J (2005) The Living Planet Index: using species population time series to track trends in biodiversity. Philos Trans R Soc B 360(1454):289–295
Macdonald DW, Burnham D, Hinks AE, Wrangham R (2013) A problem shared is a problem reduced: Seeking efficiency in the conservation of felids and primates. Folia Primatol 83(3–6):171–215
Maisels F (2001). Nouabale-Ndoki National Park, Republic du Congo, Management Plan. 2001–2006. C. d. l. P. e. d. R. H. Ministere de l'Economie Forestiere, Republique du Congo, Wildlife Conservation Society
Maisels F, Strindberg S, Blake S, Wittemyer G, Hart J, Williamson EA, Aba’a R, Abitsi G, Ambahe RD, Amsini F, Bakabana PC, Hicks TC, Bayogo RE, Bechem M, Beyers RL, Bezangoye AN, Boundja P, Bout N, Akou ME, Bene LB, Fosso B, Greengrass E, Grossmann F, Ikamba-Nkulu C, Ilambu O, Inogwabini B-I, Iyenguet F, Kiminou F, Kokangoye M, Kujirakwinja D, Latour S, Liengola I, Mackaya Q, Madidi J, Madzoke B, Makoumbou C, Malanda G-A, Malonga R, Mbani O, Mbendzo VA, Ambassa E, Ekinde A, Mihindou Y, Morgan BJ, Motsaba P, Moukala G, Mounguengui A, Mowawa BS, Ndzai C, Nixon S, Nkumu P, Nzolani F, Pintea L, Plumptre A, Rainey H, de Semboli BB, Serckx A, Stokes E, Turkalo A, Vanleeuwe H, Vosper A, Warren Y (2013) Devastating decline of forest elephants in central Africa. PLOS ONE 8(3):e59469
Mambeya MM, Baker F, Momboua BR, Koumba Pambo AF, Hega M, Okouyi Okouyi VJ, Onanga M, Challender DWS, Ingram DJ, Wang H, Abernethy K (2018) The emergence of a commercial trade in pangolins from Gabon. Afr J Ecol 56(3):601–609
Marrocoli S, Nielsen MR, Morgan D, van Loon T, Kulik L, Kühl H (2019) Using wildlife indicators to facilitate wildlife monitoring in hunter-self monitoring schemes. Ecol Ind 105:254–263
McComie LD, Dhanarajan G (1993) The physical and chemical composition of mounds of Macrotermes carbonarius (Hagen) (Termitidae, Macrotermitinae), in Penang. Malaysia J Soil Sci 44(3):427–433
Mittermeier RA (1986) Primate conservation priorities in the Neotropical region. In: Benirschke E (ed) Primates—the road to self-sustaining populations. Springer, New York, pp 221–240
Mittermeier RA (1988) Primate diversity and the tropical forest. In: Wilson EO (ed) Biodiversity. National Academy Press, Washington DC, pp 145–154
Mockrin MH (2008) The spatial structure and sustainability of subsistence wildlife harvesting in Kabo, Congo. PhD thesis. Columbia University
Mockrin MH (2010) Duiker demography and dispersal under hunting in Northern Congo. Afr J Ecol 48(1):239–247
Moe SR, Mobaek R, Narmo AK (2009) Mound building termites contribute to savanna vegetation heterogeneity. Plant Ecol 202:31–40
Morgan D, Sanz C, Onononga JR, Strindberg S (2006) Ape abundance and habitat use in the Goualougo Triangle, Republic of Congo. Int J Primatol 27(1):147–179
Morgan D, Strindberg S, Winston W, Stephens CR, Traub C, Ayina CE, Ndolo Ebika ST, Mayoukou W, Koni D, Iyenguet F, Sanz CM (2019) Impacts of selective logging and associated anthropogenic disturbance on intact forest landscapes and apes of northern Congo. Front Forest Glob Change 2(28). https://doi.org/10.3389/ffgc.2019.00028
Mugerwa B, Sheil D, Ssekiranda P, van Heist M, Ezuma P (2013) A camera trap assessment of terrestrial vertebrates in Bwindi Impenetrable National Park. Uganda Afr J Ecol 51(1):21–31
Nasi R, Billand A, van Vliet N (2012) Managing for timber and biodiversity in the Congo Basin. For Ecol Manage 268:103–111
Newbold T, Scharlemann JPW, Butchart SHM, Sekercioglu CH, Alkemade R, Booth H, Purves DW (2013) Ecological traits affect the response of tropical forest bird species to land-use intensity. Proc R Soc B 280(1750). https://doi.org/10.1098/rspb.2012.2131
Nichols JD, Karanth KU, O’Connell AF (2011) Science, conservation, and camera traps. In: O’Connell AF, Nichols JD, Karanth KU (eds) Camera traps in animal ecology. Springer, Tokyo
Noss A (2000) Cable snares and nets in the Central African Republic. In: Robinson J, Bennette (eds) Hunting for sustainability in tropical forests. Columbia University Press, New York, pp 282–304
O’Brien TG (2008) On the use of automated cameras to estimate species richness for large- and medium-sized rainforest mammals. Anim Conserv 11(3):179–181
O’Brien TG, Baillie JEM, Krueger L, Cuke M (2010) The wildlife picture index: monitoring top trophic levels. Anim Conserv 13(4):335–343
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara R, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) Vegan: community ecology package. 2019. R package version 2(10). https://github.com/vegandeus/vegan
Oldekop JA, Sims KRE, Karna BK, Whittingham MJ, Agrawal A (2019) Reductions in deforestation and poverty from decentralized forest management in Nepal. Nat Sustain 2(5):421–428
Ozaki K, Isono SM, Kawahara T, Iilda S, Kudo T, Fukuyama K (2006) A mechanistic approach to evaluation of umbrella species as conservation surrogates. Conserv Biol 20(5):1507–1515
Phillips HRP, Newbold T, Purvis A (2017) Land-use effects on local biodiversity in tropical forests vary between continents. Biodivers Conserv 26(9):2251–2270
Potapov P, Hansen MC, Laestadius L, Turubanova S, Yaroshenko A, Thies C, Smith W, Zhuravleva I, Komarova A, Minnemeyer S, Esipova E (2017) The last frontiers of wilderness: tracking loss of intact forest landscapes from 2000 to 2013. Sci Adv. https://doi.org/10.1126/sciadv.1600821
Poulsen JR, Clark CJ, Mavah G, Elkan PW (2009) Bushmeat supply and consumption in a tropical logging concession in Northern Congo. Conserv Biol 23(6):1597–1608
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ripple WJ, Wolf C, Newsome TM, Hoffmann M, Wirsing AJ, McCauley DJ (2017) Extinction risk is most acute for the world’s largest and smallest vertebrates. Proc Natl Acad Sci USA 114(40):10678–10683
Roberge JM, Angelstam P (2004) Usefulness of the umbrella species concept as a conservation tool. Conserv Biol 18(1):76–85
Rovero F, Martin E, Rosa M, Ahumada JA, Spitale D (2014) Estimating species richness and modelling habitat preferences of tropical forest mammals from camera trap data. PLOS ONE 9(7):1–2. https://doi.org/10.1371/journal.pone.0103300
Rowcliffe JM, Milner-Gulland EJ, Cowlishaw G (2005) Do bushmeat consumers have other fish to fry? Trends Ecol Evol 20(6):274–276
Rowcliffe JM, Kays R, Kranstauber B, Carbone C, Jansen PA (2014) Quantifying levels of animal activity using camera trap data. Methods Ecol Evol 5(11):1170–1179
Schipper AM, Hilbers JP, Meijer JR, Antao LH, Benitez-Lopez A, de Jonge MMJ, Leemans LH, Scheper E, Alkemade R, Doelman JC, Mylius S, Stehfest E, van Vuuren DP, van Zeist WJ, Huijbregts MAJ (2020) Projecting terrestrial biodiversity intactness with GLOBIO 4. Glob Change Biol 26(2):760–771
Scholes RJ, Biggs R (2005) A biodiversity intactness index. Nature 434(7029):45–49
Simberloff D (1998) Flagships, umbrellas and keystones: is single-species management passe´ in the landscape era? Biol Cons 83:247–257
Slough T, Kopas J, Urpelainen J (2021a) Satellite-based deforestation alerts with training and incentives for patrolling facilitate community monitoring in the Peruvian Amazon. Proc Natl Acad Sci 118(29):e2015171118
Slough T, Rubenson D, Levy R, Alpizar Rodriguez F, Bernedo del Carpio M, Buntaine MT, Christensen D, Cooperman A, Eisenbarth S, Ferraro PJ, Graham L, Hartman AC, Kopas J, McLarty S, Rigterink AS, Samii C, Seim B, Urpelainen J, Zhang B (2021b) Adoption of community monitoring improves common pool resource management across contexts. Proc Natl Acad Sci 118(29):e2015367118
Stokes EJ, Strindberg S, Bakabana PC, Elkan PW, Iyenguet FC, Madzoke B, Malanda GAF, Mowawa BS, Moukoumbou C, Ouakabadio FK, Rainey HJ (2010) Monitoring great ape and elephant abundance at large spatial scales: Measuring effectiveness of a conservation landscape. PLOS ONE 5(4). https://doi.org/10.1371/journal.pone.0010294
Strier KB, Melo FR, Mendes SL, Valença-Montenegro MM, Rylands AB, Mittermeier RA, Jerusalinsky L (2021) Science, policy, and conservation management for a critically endangered primate in the Atlantic Forest of Brazil. Front Conserv Sci. https://doi.org/10.3389/fcosc.2021.734183
Sun P, Umuntunundi P, Wronski T (2022) Species richness, relative abundance and occupancy of ground-dwelling mammals denote the ineffectiveness of chimpanzee as flagship species.. Mamm Biol 102(5):1835–1850
Taylor G, Scharlemann JPW, Rowcliffe M, Kumpel N, Harfoot MBJ, Fa JE, Melisch R, Milner-Gulland EJ, Bhagwat S, Abernethy KA, Ajonina AS, Albrechtsen L, Allebone-Webb S, Brown E, Brugiere D, Clark C, Colell M, Cowlishaw G, Crookes D, De Merode E, Dupain J, East T, Edderai D, Elkan P, Gill D, Greengrass E, Hodgkinson C, Ilambu O, Jeanmart P, Juste J, Linder JM, Macdonald DW, Noss AJ, Okorie PU, Okouyi VJJ, Pallier S, Poulsen JR, Riddell M, Schleicher J, Schulte-Herbruutiggen B, Starkey M, van Vliet N, Whitham C, Willcox AS, Wilkie DS, Wright JH, Coad LM (2015) Synthesising bushmeat research effort in West and Central Africa: a new regional database. Biol Cons 181:199–205
Tews J, Brose U, Grimm V, Tielbörger K, Wichmann MC, Schwager M, Jeltsch F (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J Biogeogr 31(1):79–92
Tobler MW, Carrillo-Percastegui SE, Leite Pitman R, Mares R, Powell G (2008) An evaluation of camera traps for inventorying large- and medium-sized terrestrial rainforest mammals. Anim Conserv 11(3):169–178
Traore S, Tigabu M, Ouedraogo SJ, Boussim JI, Guinko S et al (2008) Macrotermes mounds as sites for tree regeneration in a Sudanian woodland (Burkina Faso). Plant Ecol 198:285–295
van Vliet N (2018) Bushmeat crisis and cultural imperialism in wildlife management? Taking value orientations into account for a more sustainable and culturally acceptable wildmeat sector. Front Ecol Evol 6(112):1–6. https://doi.org/10.3389/fevo.2018.00112
van Vliet N, Nasi R (2008) Why do models fail to assess properly the sustainability of duiker ( Cephalophus spp.) hunting in Central Africa? Oryx 42(3):392–399
Vanthomme H, Bellé B, Forget PM (2010) Bushmeat hunting alters recruitment of large-seeded plant species in central Africa. Biotropica 42(6):672–679
Watson JEM, Evans T, Venter O, Williams B, Tulloch A, Stewart C, Thompson I, Ray JC, Murray K, Salazar A, McAlpine C, Potapov P, Walston J, Robinson JG, Painter M, Wilkie D, Filardi C, Laurance WF, Houghton RA, Maxwell S, Grantham H, Samper C, Wang S, Laestadius L, Runting RK, Silva-Chavez GA, Ervin J, Lindenmayer D (2018) The exceptional value of intact forest ecosystems. Nat Ecol Evolut 2(4):599–610
Western D (1987) Africa’s elephants and rhinos: flagships in crisis. Trends in Ecol Evol 2:343–346
Wilkie DS, Sidle JG, Boundzanga GC, Auzel P, Blake S (2001) Defaunation, not deforestation: Commercial logging and market hunting in northern Congo. In: Fimbel RA, Grajal A, Robinson JG (eds) The cutting edge conserving wildlife in logged tropical forest. Columbia University Press, New York, pp 375–399
Wilkie DS, Wieland M, Poulsen JR (2019) Unsustainable vs. sustainable hunting for food in Gabon: modeling short- and long-term gains and losses. Front Ecol Evolut. https://doi.org/10.3389/fevo.2019.00357
Wrangham RW, Hagel G, Leighton M, Marshall AJ, Waldau P, Nishida T (2008) The great ape world heritage species project. In: Stoinski TS, Steklis HD, Mehlman PT (eds) Conservation in the 21st century Gorillas as a case study. Springer, Boston, pp 282–295
Wright SJ (2003) The myriad consequences of hunting for vertebrates and plants in tropical forests. Perspect Plant Ecol Evolut Syst 6(1):73–86
WWF/LZS (2020). WWF Living Planet Report 2020-Bending the curve of biodiversity loss. W. R. E. A. Almond, G. M. and T. Petersen. Gland, Switzerland, WWF
Yasuoka H, Hirai M, Kamgaing TOW, Dzefack Z, Kamdoum EC, Bobo KS (2015) Changes in the composition of hunting catches in southeastern Cameroon: a promising approach for collaborative wildlife management between ecologists and local hunters. Ecol Soc. https://doi.org/10.5751/ES-08041-200425
Zett T, Stratford KJ, Weise FJ (2022) Inter-observer variance and agreement of wildlife information extracted from camera trap images. Biodivers Conserv 31:3019–3037
Ziegler S, Fa JE, Wohlfart C, Streit B, Jacob S, Wegmann M (2016) Mapping bushmeat hunting pressure in Central Africa. Biotropica 48(3):405–412
Acknowledgements
We are deeply appreciative of the opportunity to work in the Djéké Triangle and the Nouabalé-Ndoki National Park. This research would not have been possible without the continued support of the Ministère de l’Economie Forestière du gouvernement de la République du Congo and the Agence Congolaise de la Faune et des Aires Protégées (ACFAP). The Wildlife Conservation Society’s Congo Program and the Nouabalé-Ndoki Foundation are integral partners in this continuing research. Special thanks are due to R. Malonga, M. Gately, E. Stokes, T. Breuer, P. Ngouembe, D. Dos Santos, E. Arnhem, B. Evans and M. Ngangoue. We would also like to recognize the tireless dedication of J. R. Onononga, C. Eyana-Ayina, S. Ndolo Ebika, W. Mayoukou, S. Kialiema, J. Wawa, D. Koni, I. Singono, M. Meguessa, and the Mondika and Goualougo tracking teams. We also thank A. Mitchell and E. Claisse for their assistance in reviewing and compiling materials for the species identification guide. This work was greatly improved by input from J. Ray, F. Maisels, and J. Kingdon who generously provided expert review of particular taxa. We are also grateful to N. Radford for feedback on this manuscript. Acknowledgment of funding is due to the Arcus Foundation; the Conservation, Food and Health Foundation; Lincoln Park Zoo, Indianapolis Zoo; the Saint Louis Zoo, Woodland Park Zoo, Zoo Atlanta and the Cincinnati Zoo and Botanical Garden. In addition, we are immensely grateful to S. Ross who provided enthusiastic encouragement and support for these field conservation efforts over many years. This research would not have been possible without him.
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Conceptualization, DM, SS and CS; Methodology, DM, SS and CS; Investigation, DM, AZ, IS, SH, SM, CEA, PJ, RC and CS; Data Curation, DM, SH, SM, PM, JF, HH and CS; Writing—Original Draft Preparation, DM and CS; Writing—Review and Editing, DM, SS, PM, AZ, IS, SH, SM, CEA, JF and CS; Visualization, DM, PM and JF; Supervision, DM, AZ, CEA and CS; Project Administration, DM, AZ, CEA, HH and CS; Funding Acquisition, DM, SM, HH and CS.
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Our study adhered to the legal requirements of the Republic of Congo where the research was conducted. The research was approved by the Nouabalé-Ndoki Foundation and the Wildlife Conservation Society’s Congo Program. We also complied with ethics guidelines of the Association for the Study of Animal Behaviour (ASAB) and Animal Behavior Society. After reviewing the study’s camera trapping methods, Washington University issued an IACUC exemption.
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Morgan, D., Strindberg, S., McElmurray, P. et al. Extending the conservation impact of great ape research: Flagship species sites facilitate biodiversity assessments and land preservation. Primates (2023). https://doi.org/10.1007/s10329-023-01080-x
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DOI: https://doi.org/10.1007/s10329-023-01080-x