[en] The duiker community in Central African rainforests includes a diversity of species that
can coexist in the same area. The study of their activity patterns is needed to better understand
habitat use or association between the species. Using camera traps, we studied the temporal
activity patterns, and quantified for the first time the temporal overlap and spatial co-occurrence
between species. Our results show that: (i) Two species are strongly diurnal: Cephalophus leucogaster and Philantomba congica, (ii) two species are mostly diurnal: C. callipygus and C. nigrifrons, (iii) one species is strongly nocturnal: C. castaneus, (iv) and one species is mostly nocturnal: C. silvicultor. Analyses of temporal activities (for five species) identified four species pairs that highly overlapped (Δ ≥ 0.80), and six pairs that weakly overlapped (Δ between 0.06 and 0.35). Finally, co-occurrence tests reveal a truly random co-occurrence (plt > 0.05 and pgt > 0.05) for six species pairs, and a positive co-occurrence (pgt < 0.05) for four pairs. Positive co-occurrences are particularly noted for pairs formed by C. callipygus with the other species (except C. nigrifrons). These results are essential for a better understanding of the coexistence of duikers and the ecology of poorly known species (C. leucogaster and C. nigrifrons), and provide clarification on the activity patterns of C. silvicultor which was subject to controversy. Camera traps proved then to be a powerful tool for studying the activity patterns of free-ranging duiker populations.
Research center :
Terra Teaching and Research Centre, Forest Is life, Gembloux Agro-Bio Tech, Université de Liège
Cornelis, Daniel; French Agricultural Research Center for International Development (CIRAD), 34398 Montpellier CEDEX 5, France
Vermeulen, Cédric ; Université de Liège - ULiège > Département GxABT > Laboratoire de Foresterie des régions trop. et subtropicales
Sonké, Bonaventure; Département de Biologie, Laboratoire de Botanique Systématique et d’Écologie, École Normale Supérieure, Université de Yaoundé I, BP 047 Yaoundé, Cameroon
Ntie, Stephan; Département de Biologie, Laboratoire de Biologie Moléculaire et Cellulaire (LABMC), Université des Sciences et Techniques de Masuku (USTM), BP 941 Franceville, Gabon
Fayolle, Adeline ; Université de Liège - ULiège > Département GxABT > Gestion des ressources forestières et des milieux naturels
Fonteyn, Davy ; Université de Liège - ULiège > Département GxABT > Gestion des ressources forestières et des milieux naturels
Lhoest, Simon ; Université de Liège - ULiège > Département GxABT > Gestion des ressources forestières et des milieux naturels
Yapi, Fabrice; Office Ivoirien des Parcs et Réserves, Yamoussoukro 225, Cote D’Ivoire
Sandrin, François; Independent Consultants, Center for International Forestry Research (CIFOR), Situ Gede, Bogor Barat, Bogor Jawa 16115, Barat, Indonesia
Vanegas, Liliana; Independent Consultants, Center for International Forestry Research (CIFOR), Situ Gede, Bogor Barat, Bogor Jawa 16115, Barat, Indonesia
Ayaya, Idriss; Faculté des Sciences Agronomiques, Université de l’Uélé, Haut-Uélé, Isiro BP 670, Congo
Hardy, Clément; Department of Biological Sciences, UQAM, Montréal, QC H3W 1R7, Canada
Le Bel, Sebastien; French Agricultural Research Center for International Development (CIRAD), 34398 Montpellier CEDEX 5, France
Doucet, Jean-Louis ; Université de Liège - ULiège > Département GxABT > Laboratoire de Foresterie des régions trop. et subtropicales
Hempson, G.P.; Archibald, S.; Bond, W.J.A. Continent-Wide Assessment of the Form and Intensity of Large Mammal Herbivory in Africa. Science 2015, 350, 1056–1061. [CrossRef] [PubMed]
Van Vuuren, B.J.; Robinson, T.J. Retrieval of Four Adaptive Lineages in Duiker Antelope: Evidence from Mitochondrial DNA Sequences and Fluorescence in Situ Hybridization. Mol. Phylogenet. Evol. 2001, 20, 409–425. [CrossRef] [PubMed]
Ntie, S.; Johnston, A.R.; Mickala, P.; Bowkett, A.E.; Jansen van Vuuren, B.; Colyn, M.; Telfer, P.; Maisels, F.; Hymas, O.; Rouyer, R.L.; et al. Molecular Diagnostic for Identifying Central African Forest Artiodactyls from Faecal Pellets. Anim. Conserv. 2010, 13, 80–89. [CrossRef]
Johnston, A.R.; Anthony, N.M.A. Multi-Locus Species Phylogeny of African Forest Duikers in the Subfamily Cephalophinae: Evidence for a Recent Radiation in the Pleistocene. BMC Evol. Biol. 2012, 12, 1–16. [CrossRef] [PubMed]
Groves, C.; Grubb, P. Ungulate Taxonomy; Johns Hopkins University Press: Baltimore, ML, USA, 2011; p. 317.
Fimbel, C.; Curran, B.; Usongo, L. Enhancing the sustainability of duiker hunting through community participation and controlled access in the Lobéké region of southeastern Cameroon. In Hunting for Sustainability in Tropical Forest; Robinson, J.G., Bennett, E.L., Eds.; Colombia University Press: New York, NY, USA, 2000; pp. 356–374.
Van Vliet, N.; Zundel, S.; Miquel, C.; Taberlet, P.; Nasi, R. Distinguishing Dung from Blue, Red and Yellow-Backed Duikers through Noninvasive Genetic Techniques. Afr. J. Ecol. 2007, 46, 411–417. [CrossRef]
Ghassemi-Khademi, T.; Hamidi, K. Re-Evaluation of Molecular Phylogeny of the Subfamily Cephalophinae (Bovidae: Artiodactyla); with Notes on Diversification of Body Size. Jordan J. Biol. Sci. 2019, 12, 637–647.
Castelló, J.R. Bovids of the World: Antelopes, Gazelles, Cattle, Goats, Sheep, and Relatives; Princeton University Press: Princeton, NJ, USA, 2016; Volume 104, p. 665.
Hedwig, D.; Kienast, I.; Bonnet, M.; Curran, B.K.; Courage, A.; Boesch, C.; Kühl, H.S.; King, T. A Camera Trap Assessment of the Forest Mammal Community within the Transitional Savannah-Forest Mosaic of the Batéké Plateau National Park, Gabon. Afr. J. Ecol. 2018, 56, 777–790. [CrossRef]
Mockrin, M.H. Duiker Demography and Dispersal under Hunting in Northern Congo. Afr. J. Ecol. 2010, 48, 239–247. [CrossRef]
Yasuoka, H.; Hirai, M.; Kamgaing, T.O.W.; Dzefack, Z.C.B.; Kamdoum, E.C.; Bobo, K.S. Changes in the Composition of Hunting Catches in Southeastern Cameroon: A Promising Approach for Collaborative Wildlife Management between Ecologists and Local Hunters. Ecol. Soc. 2015, 20. [CrossRef]
Vanthomme, H.; Bellé, B.; Forget, P.-M. Bushmeat Hunting Alters Recruitment of Large-Seeded Plant Species in Central Africa. Biotropica 2010, 42, 672–679. [CrossRef]
Newing, H. Bushmeat Hunting and Management: Implications of Duiker Ecology and Interspecific Competition. Biodivers. Conserv. 2001, 10, 99–118. [CrossRef]
Azevedo, F.C.; Lemos, F.G.; Freitas-Junior, M.C.; Rocha, D.G.; Azevedo, F.C.C. Puma Activity Patterns and Temporal Overlap with Prey in a Human-Modified Landscape at Southeastern Brazil. J. Zool. 2018, 305, 246–255. [CrossRef]
Kneitel, J.M.; Chase, J.M. Trade-Offs in Community Ecology: Linking Spatial Scales and Species Coexistence. Ecol. Lett. 2004, 7, 69–80. [CrossRef]
Johnson, D.H. The Comparison of Usage and Availability Measurements for Evaluating Resource Preference. Ecology 1980, 61, 65–71. [CrossRef]
Halle, S.; Stenseth, N.C. (Eds.) Introduction. In Activity Patterns in Small Mammals—An Ecological Approach; Springer: Berlin, Germany, 2000; Volume 141, pp. 3–17.
Bennie, J.J.; Duffy, J.P.; Inger, R.; Gaston, K.J. Biogeography of Time Partitioning in Mammals. Proc. Natl. Acad. Sci. USA 2014, 111, 13727–13732. [CrossRef]
Ridout, M.S.; Linkie, M. Estimating overlap of daily activity patterns from camera trap data. J. Agric. Biol. Environ. Stat. 2009, 14, 322–337. [CrossRef]
Weitzman, M.S. Measures of the Overlap of Income Distribution of White and Negro Families in the United States; Bureau of the Census: Washington, DC, USA, 1970; Volume 22.
Veech, J.A.A. Probabilistic Model for Analysing Species Co-Occurrence. Glob. Ecol. Biogeogr. 2013, 22, 252–260. [CrossRef]
Rota, C.T.; Ferreira, M.A.R.; Kays, R.W.; Forrester, T.D.; Kalies, L.; Mcshea, W.J.; Parsons, A.W.; Millspaugh, J.J. A Multispecies Occupancy Model for Two or More Interacting Species. Methods Ecol. Evol. 2016, 7, 1164–1173. [CrossRef]
Bourgoin, G.; Garel, M.; Blanchard, P.; Dubray, D.; Maillard, D.; Gaillard, J.M. Daily Responses of Mouflon (Ovis Gmelini Musimon × Ovis Sp.) Activity to Summer Climatic Conditions. Can. J. Zool. 2011, 89, 765–773. [CrossRef]
Frey, S.; Fisher, J.T.; Burton, A.C.; Volpe, J.P. Investigating Animal Activity Patterns and Temporal Niche Partitioning Using Camera-Trap Data: Challenges and Opportunities. Remote Sens. Ecol. Conserv. 2017, 3, 123–132. [CrossRef]
Saint-Girons, M.C. Le rythme circadian d’activité chez les mammifères holarctiques. Mém. Mus. Natl. Hist. Nat. Sér. A Zool. 1966, 40, 101–187. (In French)
Johnsingh, T.A.J. Large Mammalian Prey-Predators in Bandipur. J. Bombay Nat. Hist. Soc. 1983, 80, 1–57.
Bowland, A.E.; Perrin, M.R. Temporal and Spatial Patterns in Blue Duikers Philatomba Monticola and Red Duikers Cephalophus natalensis. J. Zool. 1995, 237, 487–498. [CrossRef]
Dubost, G. L‘écologie et La Vie Sociale Du Céphalophe Bleu (Cephalophus Monticola Thunberg), Petit Ruminant Forestier Africain. Z. Tierpsychol. 1980, 54, 205–266. [CrossRef]
Bessone, M.; Kühl, H.S.; Hohmann, G.; Herbinger, I.; N’Goran, K.P.; Asanzi, P.; da Costa, P.B.; Dérozier, V.; Fotsing, E.D.B.; Beka, B.I.; et al. Drawn out of the Shadows: Surveying Secretive Forest Species with Camera Trap Distance Sampling. J. Appl. Ecol. 2020, 57, 963–974. [CrossRef]
Harmsen, B.J.; Foster, R.J.; Silver, S.C.; Ostro, L.E.T.; Doncaster, C.P. Jaguar and Puma Activity Patterns in Relation to Their Main Prey. Mamm. Biol. 2011, 76, 320–324. [CrossRef]
Feer, F. Stratégies Écologiques de Deux Espèces de Bovidés Sympatriques de La Forêt Sempervirente Africaine (Cephalophus Callipygus et C. Dorsalis): Influence du rythme d’activité. Ph.D. Thesis, Université Pierre et Marie Curie, Paris, France, 1988. (In French).
Feer, F. Comparaison Des Régimes Alimentaires de Cephalophus Callipygus et C. Dorsalis. Bovidés Sympatriques de La Forêt Sempervirente Africaine. Mammalia 1989, 53, 563–604. [CrossRef]
Kranz, K.R.; Lumpkin, S. Notes on the yellow-backed duiker Cephalophus sylvicultor in captivity with comments on its natural history. Int. Zoo Yearb. 1982, 22, 232–240. [CrossRef]
Gessner, J.; Buchwald, R.; Wittemyer, G. Assessing Species Occurrence and Species-Specific Use Patterns of Bais (Forest Clearings) in Central Africa with Camera Traps. Afr. J. Ecol. 2014, 52, 59–68. [CrossRef]
Nakashima, Y.; Hongo, S.; Akomo-Okoue, E.F. Landscape-Scale Estimation of Forest Ungulate Density and Biomass Using Camera Traps: Applying the REST Model. Biol. Conserv. 2020, 241, e108381. [CrossRef]
Illius, A.W.; Gordon, I.J. Modelling the Nutritional Ecology of Ungulate Herbivores: Evolution of Body Size and Competitive Interactions. Oecologia 1992, 89, 428–434. [CrossRef] [PubMed]
White, F. The vegetation of Africa: A descriptive memoir to accompany the UNESCO/AETFAT/UNSO vegetation map of Africa. Nat. Resour. Res. 1983, 20, 351–356.
Gond, V.; Fayolle, A.; Pennec, A.; Cornu, G.; Mayaux, P.; Camberlin, P.; Doumenge, C.; Fauvet, N.; Gourlet-Fleury, S. Vegetation Structure and Greenness in Central Africa from Modis Multi-Temporal Data. Philos. Trans. R. Soc. B: Biol. Sci. 2013, 368, e20120309. [CrossRef]
Van Schaik, C.P.; Griffiths, M. Activity Periods of Indonesian Rain Forest Mammals. Biotropica 1996, 28, e105. [CrossRef]
Noor, A.; Mir, Z.R.; Veeraswami, G.G.; Habib, B. Activity Patterns and Spatial Co-Occurrence of Sympatric Mammals in the Moist Temperate Forest of the Kashmir Himalaya, India. Folia Zool. 2017, 66, 231–241. [CrossRef]
Camera Base. Available online: http://www.atrium-biodiversity.org/tools/camerabase/(accessed on 4 June 2019).
Groves, C.P.; Leslie, D.M., Jr. Family Bovidae (hollow-horned ruminants). In Handbook of the Mammals of the World, 2nd ed.; Wilson, D.E., Mittermeier, R.A., Eds.; Lynx Edicions: Barcelona, Spain, 2011; Volume 2, pp. 755–773.
Caravaggi, A.; Gatta, M.; Vallely, M.C.; Hogg, K.; Freeman, M.; Fadaei, E.; Dick, J.T.A.; Montgomery, W.I.; Reid, N.; Tosh, D.G. Seasonal and Predator-Prey Effects on Circadian Activity of Free-Ranging Mammals Revealed by Camera Traps. PeerJ 2018, 6, e5287. [CrossRef] [PubMed]
Cusack, J.J.; Dickman, A.J.; Rowcliffe, J.M.; Carbone, C.; Macdonald, D.W.; Coulson, T. Random versus Game Trail-Based Camera Trap Placement Strategy for Monitoring Terrestrial Mammal Communities. PLoS ONE 2015, 10, e0126373. [CrossRef] [PubMed]
Cruz, P.; Iezzi, M.E.; de Angelo, C.; Varela, D.; di Bitetti, M.S.; Paviolo, A. Effects of Human Impacts on Habitat Use, Activity Patterns and Ecological Relationships among Medium and Small Felids of the Atlantic Forest. PLoS ONE 2018, 13, e0200806. [CrossRef]
Hansen, M.C.; Potapov, P.V.; Moore, R.; Hancher, M.; Turubanova, S.A.; Tyukavina, A.; Thau, D.; Stehman, S.V.; Goetz, S.J.; Loveland, T.R.; et al. High-Resolution Global Maps of 21st-Century Forest Cover Change. Science 2013, 342, 850–853. [CrossRef] [PubMed]
USNO. Available online: https://aa.usno.navy.mil/faq/docs/world_tzones.php. (accessed on 4 April 2019).
Gómez, H.; Wallace, R.B.; Ayala, G.; Tejada, R. Dry Season Activity Periods of Some Amazonian Mammals. Stud. Neotrop. Fauna Environ. 2005, 40, 91–95. [CrossRef]
Ross, J.; Hearn, A.J.; Johnson, P.J.; Macdonald, D.W. Activity patterns and temporal avoidance by prey in response to Sunda clouded leopard predation risk. J. Zool. Lond. 2013, 290, 96–106. [CrossRef]
Pewsey, A.; Neuhäuser, M.; Ruxton, G.D. Circular Statistics in R, 1st ed.; Oxford University Press: New York, NY, USA, 2013; p. 183.
Landler, L.; Ruxton, G.D.; Malkemper, E.P. The Hermans-Rasson Test as a Powerful Alternative to the Rayleigh Test for Circular Statistics in Biology. BMC Ecol. 2019, 19. [CrossRef]
Fernández-Durán, J.J. Circular Distributions Based on Nonnegative Trigonometric Sums. Biometrics 2004, 60, 499–503. [CrossRef]
Linkie, M.; Ridout, M.S. Assessing Tiger-Prey Interactions in Sumatran Rainforests. J. Zool. 2011, 284, 224–229. [CrossRef]
Monterroso, P.; Alves, P.C.; Ferreras, P. Plasticity in Circadian Activity Patterns of Mesocarnivores in Southwestern Europe: Implications for Species Coexistence. Behav. Ecol. Sociobiol. 2014, 68, 1403–1417. [CrossRef]
Overview of the Overlap Package. Available online: https://cran.r-project.org/web/packages/overlap/vignettes/overlap.pdf (accessed on 18 July 2019).
Havmøller, R.W. Assessing the Activity Pattern Overlap among Leopards (Panthera Pardus), Potential Prey and Competitors in a Complex Landscape in Tanzania. J. Zool. 2020, 311, 175–182. [CrossRef]
Griffith, D.M.; Veech, J.A.; Marsh, C.J. Cooccur: Probabilistic Species Co-Occurrence Analysis in R. J. Stat. Softw. 2016, 69. [CrossRef]
The R Project for Statistical Computing. Available online: https://www.r-project.org/(accessed on 10 April 2016).
Dray, S.; Dufour, A.B. The Ade4 Package: Implementing the Duality Diagram for Ecologists. J. Stat. Softw. 2007, 22, 1–20. [CrossRef]
Package ‘CircMLE’. Available online: https://cran.r-project.org/web/packages/CircMLE/CircMLE.pdf (accessed on 28 October 2020).
Package ‘Circular’. Available online: https://cran.r-project.org/web/packages/circular/circular.pdf (accessed on 10 May 2019).
Package ‘Activity’. Available online: https://cran.r-project.org/web/packages/activity/activity.pdf (accessed on 4 September 2020).
Kingdon, J. The Kingdon Field Guide to African Mammals, 2nd ed.; Bloomsbury Publishing: London, UK, 2015.
Mori, E.; Nerva, L.; Lovari, S. Reclassification of the Serows and Gorals: The End of a Neverending Story? Mamm. Rev. 2019, 49, 256–262. [CrossRef]
Stockman, A.; Sharpe, L.T. Into the Twilight Zone: The Complexities of Mesopic Vision and Luminous Efficiency. Ophthal. Physl. opt. 2006, 26, 225–239. [CrossRef]
Dubost, G. The Size of African Forest Artiodactyls as Determined by the Vegetation Structure. Afr. J. Ecol. 1979, 17, 1–17. [CrossRef]
Kingdon, J.; Lahm, S.A. Cephalophus silvicultor Yellow-backed Duiker. In Mammals of Africa: Volume VI: Pigs, Hippopotamuses, Chevrotain, Giraffes, Deer and Bovids; Kingdon, J., Hoffmann, M., Eds.; Bloomsbury Publishing: London, UK, 2013; Volume 6, pp. 288–293.
De Sá Alves, L.C.P.; Andriolo, A. Camera traps used on the mastofaunal survey of Araras Biological Reserve. IEF-RJ. Rev. Bras. Zoociências 2005, 7, 231–246.
Lahm, S.A. Ecology and Economics of Human/Wildlife Interaction in North-East Gabon. Ph.D. Thesis, New York University, New York, NY, USA, 1993.
Croes, B.M.; Laurance, W.F.; Lahm, S.A.; Tchignoumba, L.; Alonso, A.; Lee, M.E.; Campbell, P.; Buij, R. The Influence of Hunting on Antipredator Behavior in Central African Monkeys and Duikers. Biotropica 2007, 39, 257–263. [CrossRef]
Gautier-Hion, A.; Gautier, J.-P. Cephalophus ogilbyi crusalbum Grubb 1978, described from coastal Gabon, is quite common in the forêt des abeilles, central Gabon. Rev. Ecol. 1994, 49, 177–180.
Houngbégnon, F.G.A.; Sonké, B.; Vermeulen, C.; Doucet, J.L. State of Knowledge on Duikers (Genera Cephalophus and Philantomba) of Central Africa Rainforests. A Review. Biotechnol. Agron. Soc. Environ. 2019, 23, 104–124.
Veech Research Group in Ecology. Available online: http://ecology.wp.txstate.edu/publications-2/(accessed on 28 October 2019).
