Flexibility in behavior and ecology

Funding: DAAD, Konrad-Adenauer-Stiftung and external through collaboration

Project Details:
The proboscis monkey (Nasalis larvatus) is a large-bodied folivorous primate, forming harem and bachelor groups in lowland tropical rainforests in Borneo. Due to anthropogenic habitat loss and fragmentation, this primate species is highly endangered, and a better knowledge of their behavior and health status may improve their conservation and management. The goal of this project is to study its superficially known vocal signalling system and its intestinal parasite load to evaluate negative consequences of habitat fragmentation and the zoonotic risks that need to be considered when designing effective management programs. We investigate and compare those aspects in one-male (harem) and all-male (bachelor) groups in the Lower Kinabatangan Wildlife Sanctuary, Borneo, as well as in the Labuk Bay Sanctuary to study the role of vocalizations in governing spacing and cohesion. Furthermore, we assess intestinal parasite communities to link them to social grouping pattern and communication and to get insight into their significance for zoonotic diseases.

Results:

e.g.:

Scheumann, M., Röper, K. M., Nathan, S. K., & Goossens, B. (2022): Third-party vocal intervention in the proboscis monkey (Nasalis larvatus). Int. J. Primatol., 43: 1-14. https://doi.org/10.1007/s10764-021-00273-9

 

Klaus, A.; Strube, C.; Röper, K. M.; Radespiel, U.; Schaarschmidt, F.; Nathan, S.; Goossens, B.; Zimmermann, E.(2018): Fecal parasite risk in the endangered proboscis monkey is higher in an anthropogenically managed forest environment compared to a riparian rain forest in Sabah, Borneo in PlosOne 13(4). https:// doi.org/10.1371/journal.pone.0195584

 

Klaus, A.; Zimmermann, E.; Röper, K.M.; Radespiel, U.; Nathan, S.; Goossens, B.; Strube, C. (2017): Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus)in Borneo.Int. Journ. for Parasitology: Parasites and Wildlife. 6(3): 320-329. https.//10.1016/j.ijppaw.2017.09.005

 

Röper, K.M.; Scheumann, M.; Wiechert, A.B.; Nathan, S.; Goossens, B.; Owren, M.J.; Zimmermann, E. (2014): Vocal acoustics in the endangered proboscis monkey (Nasalis larvatus). Am. J. Primatol. 76 (2): 192-201. https://doi.org/10.1002/ajp.22221

Cooperation Partners:

Dr. Benoit Goossens, Danau Girang Field Center, Malaysia, and Cardiff University, GB

Dr. Ikki Matsuda, Primate Research Center, Inumyama, Japan

Dipl. Biol. Kathrin M. Röper, Zoo Hannover

Funding: Volkswagen Stiftung, external funding through cooperation, 148.400 EUR

Project Details:
Die Sensitivität und Spezifität der Pheromonwahrnehmung hängt von den Rezeptoren im Epithelium des VNOs ab. Es wurden bisher zwei Familien von VNO Rezeptoren identifiziert, V1R und V2R. Die Diversität von VNO Rezeptoren ist in den verschiedenen Primatenfamilien wenig untersucht. Das Verständnis der Evolution des VNO ist entscheidend, um die adaptiven Veränderungen der relativen Relevanz verschiedener Sinnessysteme während der Evolution der Primaten zu verstehen. Aufgrund der zunehmenden Degeneration des VNOs und der Pseudogenisierung der V1R Gene bei höheren Affen ereignete sich die adaptive Evolution dieser Gene vermutlich sehr früh innerhalb der Stammesgeschichte der Primaten. Innerhalb dieses Forschungsprojekts werden die funktionellen VNO-Rezeptorgene von basalen Primaten, den Mausmakis (Microcebus spp.), isoliert und hinsichtlich ihrer Variabilität, Selektion und phylogenetischen Bedeutung chrakterisiert. Zudem werden die olfaktorischen Markiersubstanzen hinsichtlich ihrer potentiell signalgebenden Komponenten untersucht und Bioessays zur olfaktorischen Wahrnehmungsleistung von Mausmakis entwickelt.

Results:

e.g.

 

Kollikowski, A.; Jeschke, S.; Radespiel, U. (2020): Experimental evaluation of spontaneous olfactory discrimination in two nocturnal primates (Microcebus murinus and M. lehilahytsara). Chemical Senses, 45, 581-592. bjaa051. https://doi.org/10.1093/chemse/bjaa051

 

Caspers, J.; Radespiel, U.; Zimmermann, E. Schulz, S. (2020): Volatile urinary signals of two nocturnal primates, Microcebus murinus and M. lehilahytsara. Frontiers Ecology and Evolution, 8, 158. https://doi.org/10.3389/fevo.2020.00158

 

Kollikowski, A.; Zimmermann, E.; Radespiel, U. (2019): First experimental evidence for olfactory species discrimination in two nocturnal primate species (Microcebus lehilahytsara and M. murinus). Sci. Rep., 9, 20386. http://doi.org/10.1038/s41598-019-56893-y.

 

Unsworth, J.; Loxley, G.; Davidson, A.; Hurst, J.L.; Gomez-Baena, G.; Mundy, N.I.; Beynon, R.; Zimmermann, E. and Radespiel, U. (2017): Characterisation of urinary WFDC12 in small nocturnal basal primates, mouse lemurs (Microcebus spp.). Scientific Reports, 7, 42940. doi:10.1038/srep42940.

 

Hohenbrink, P.; Mundy, N.I.; Radespiel, U. (2017): Population genetics of mouse lemur vomeronasal receptors: current versus past selection and demographic inferences. BMC Evol.Biol., DOI: 10.1186/s12862-017-0874-6.

Cooperation Partners:

Dr. Nick Mundy, Cambridge University, UK

Prof. Jane Hurst, University of Liverpool, UK

Prof. Rob Beynon, University of Liverpool, UK

Prof. Dr. S. Schulz, TU Braunschweig

Prof. Dr. Markus Rothermel, Universität Magdeburg

Funding: DFG (RA 502/20-1 and others), Volkswagen-Stiftung, DAAD (PhD/reinvitation fellowship to BR, SR, RoR, RiR, AH), private donors, Biopat e.V.; Small Rufford Fund

Project Details:
A central question in evolutionary and conservation biology is how and to what extent species adapt to habitat fluctuations in their natural environment and to what extent environmental flexibility is linked to distribution and speciation. We address these questions in a longterm research programme by a comparative and integrative approach to nocturnal lemurs, a unique model for basal primates. Lemurs are endemic to Madagascar. Current research revealed a much higher species diversity in nocturnal lemurs than previously assumed. Lemurs underwent a broad-scale adaptive radiation after their initial colonization of Madagascar about 60 Mya. Extant lemurs consist of more than 100 species which inhabit the various forest habitats of the Island. Many species, in particular nocturnal species, have only been described recently, partly by our group. The underlying colonisation history and the factors driving this diversification are so far only poorly known. Here, we aim to understand the factors that promoted this radiation and shaped distribution, adaptation and genetic structures of lemurs. We are also addressing the question of the basis of reproductive isolation of species. These analyses are focused on the genera Microcebus spp., Lepilemur spp. and Avahi ssp. Whereas some species within a taxon show quite limited, others show broad distributions. Nocturnal lemurs belong to the endangered primates due to anthopogenically caused habitat degradation and poaching. We perform field studies, supplemented by experimental studies, particulary in north-western, northern and eastern Madagascar, using comparable methods, to study the ecology, behaviour, communication, parasite infections and the genetics of populations of lemurs of the same taxon showing contrasting distribution and to assess sensory, vocal, ecological and social determinants of species flexibility and its link to genetics. Our current research focus is on mouse lemurs, sportive lemurs and woolly lemurs. Results will deliver important tools to monitor and manage the biodiversity in tropical forests. Furthermore they will be a first step to understand the evolution of the unique species diversity of lemurs in Madagascar and the origin and evolution of our own primate ancestry.

Results:

e.g.

Ganzhorn, J.U.; Ratovonamana, Y.R.; Rother, M.; Giertz, P.; Andrews, C.A.; Baumann, S.; Bohr, Y.E.-M.B.; Kappeler, P.M.; Montero, K.B.; Pommerening-Roeser, A.; Radespiel, U.; Rakotondranary, J.S.; Schülke, O.; Steffens, K.J.E.; Thorén, S.; Timmermann, G.; Tomaschewski, I. (2023): Nutritional and possible pharmaceutical aspects of tree exudates eaten by lemurs of Madagascar?s dry forests. Separations, 10, 575. https:// doi.org/10.3390/separations10110575

 

Schüßler, D.; Blanco, M.B.; Guthrie, N.K.; Sgarlata, G.M.; Dammhahn, M.; Refaly, E.; Rina Evasoa, M.; Hasiniaina, A.; Hending, D.; Jan, F.; le Pors, B.; Miller, A.; Olivieri, G.; Rakotonanahary, A.N.; Rakotondranary, S.J.; Rakotondravony, R.; Ralantoharijaona, T.; Ramananjato, V.; Randrianambinina, B.; Raoelinjanakolona, N.N.; Rasoazanabary, E.; Rasoloarison, R.M.; Rasolofoson, D.W.; Rasoloharijaona, S.; Rasolondraibe, E.; Roberts, S.H.; Teixeira, H.; van Elst, T.; Johnson, S.E.; Ganzhor, J.U.; Chikhi, L.; Kappeler, P.M.; Louis Jr., E.E.; Salmona, J.; Radespiel, U. (2023): Morphological variability or inter-observer bias? A methodological toolkit to improve data quality of multi-researcher datasets for the analysis of morphological variation. Am. J. of Biol. Anthropol., 183, 60-78. https://doi.org/10.1002/ajpa.24836

 

Marquès Gomila, C.; Kiene, F.; Klein, A.; Kessler, S.E.; Zohdy, S.; Rakotondravony, R.; Durden, L.A.; Radespiel, U. (2023): Host-related and environmental factors influence long-term ectoparasite infestation dynamics of mouse lemurs in northwestern Madagascar. Am. J. Primatol., 85(6), e23494. https://doi.org/10.1002/ajp.23494

 

Springer, A.; Durden L.A.; Kiene F.; Klein, A.; Rakotondravony, R.; Ehlers, J.; Greiman, S.E.; Blanco, M.B.; Zohdy, S.; Kessler, S.E.; Strube, C.*; Radespiel, U.* (2023): Molecular phylogenetics of the sucking louse genus Lemurpediculus (Insecta: Phthiraptera), ectoparasites of lemurs, with descriptions of three new species. International Journal for Parasitology: Parasites and Wildlife, 20, 138-152. https://doi.org/10.1016/j.ijppaw.2023.02.002 (*: joint senior authors)

 

Kessler, S.; Tsangaras, K.; Rasoloharijaona, S.; Radespiel, U.; Greenwood, A.D. (2023): Long-term host-pathogen evolution of endogenous beta- and gammaretroviruses in mouse lemurs with little evidence of recent retroviral introgression. Virus Evolution, 9, 1-13. DOI: https://doi.org/10.1093/ve/veac117

Cooperation Partners:

Prof. Dr. Blanchard Randrianbinina (BR), Université de Mahajanga, Madagascar

Prof. Dr. Solofonirina Rasoloharijaona (SR), Université de Mahajanga, Madagascar

Dr. Romule Rasoloarison (RoR), Université de Mahajanga, Madagascar

Dr. Rindra Ramanankirahina (RiR), Université de Antananrivo, Madagascar

Alida Hasinianina, PhD, Madagascar

Mamy R. Evasoa, PhD, University of Mahajanga, Madagascar

Dr. L. Chikhi, Toulouse University, France and IGC, Portugal

Prof. B. Crowley, University of Cincinnati, USA

Groupe d'Étude et de Recherche sur les Primates de Madagascar

Prof. J. Ratsimbazafy, University of Antananarivo, Madagascar

Funding: DFG (RA 502/20-1 and others), Volkswagen-Stiftung, DAAD (PhD/reinvitation fellowship to BR, SR, RoR, RiR, AH), private donors, Biopat e.V.; Small Rufford Fund

Project Details:
A central question in evolutionary and conservation biology is how and to what extent species adapt to habitat fluctuations in their natural environment and to what extent environmental flexibility is linked to distribution and speciation. We address these questions in a longterm research programme by a comparative and integrative approach to nocturnal lemurs, a unique model for basal primates. Lemurs are endemic to Madagascar. Current research revealed a much higher species diversity in nocturnal lemurs than previously assumed. Lemurs underwent a broad-scale adaptive radiation after their initial colonization of Madagascar about 60 Mya. Extant lemurs consist of more than 100 species which inhabit the various forest habitats of the Island. Many species, in particular nocturnal species, have only been described recently, partly by our group. The underlying colonisation history and the factors driving this diversification are so far only poorly known. Here, we aim to understand the factors that promoted this radiation and shaped distribution, adaptation and genetic structures of lemurs. We are also addressing the question of the basis of reproductive isolation of species. These analyses are focused on the genera Microcebus spp., Lepilemur spp. and Avahi ssp. Whereas some species within a taxon show quite limited, others show broad distributions. Nocturnal lemurs belong to the endangered primates due to anthopogenically caused habitat degradation and poaching. We perform field studies, supplemented by experimental studies, particulary in north-western, northern and eastern Madagascar, using comparable methods, to study the ecology, behaviour, communication, parasite infections and the genetics of populations of lemurs of the same taxon showing contrasting distribution and to assess sensory, vocal, ecological and social determinants of species flexibility and its link to genetics. Our current research focus is on mouse lemurs, sportive lemurs and woolly lemurs. Results will deliver important tools to monitor and manage the biodiversity in tropical forests. Furthermore they will be a first step to understand the evolution of the unique species diversity of lemurs in Madagascar and the origin and evolution of our own primate ancestry.

Results:

e.g.

Ganzhorn, J.U.; Ratovonamana, Y.R.; Rother, M.; Giertz, P.; Andrews, C.A.; Baumann, S.; Bohr, Y.E.-M.B.; Kappeler, P.M.; Montero, K.B.; Pommerening-Roeser, A.; Radespiel, U.; Rakotondranary, J.S.; Schülke, O.; Steffens, K.J.E.; Thorén, S.; Timmermann, G.; Tomaschewski, I. (2023): Nutritional and possible pharmaceutical aspects of tree exudates eaten by lemurs of Madagascar?s dry forests. Separations, 10, 575. https:// doi.org/10.3390/separations10110575

 

Schüßler, D.; Blanco, M.B.; Guthrie, N.K.; Sgarlata, G.M.; Dammhahn, M.; Refaly, E.; Rina Evasoa, M.; Hasiniaina, A.; Hending, D.; Jan, F.; le Pors, B.; Miller, A.; Olivieri, G.; Rakotonanahary, A.N.; Rakotondranary, S.J.; Rakotondravony, R.; Ralantoharijaona, T.; Ramananjato, V.; Randrianambinina, B.; Raoelinjanakolona, N.N.; Rasoazanabary, E.; Rasoloarison, R.M.; Rasolofoson, D.W.; Rasoloharijaona, S.; Rasolondraibe, E.; Roberts, S.H.; Teixeira, H.; van Elst, T.; Johnson, S.E.; Ganzhor, J.U.; Chikhi, L.; Kappeler, P.M.; Louis Jr., E.E.; Salmona, J.; Radespiel, U. (2023): Morphological variability or inter-observer bias? A methodological toolkit to improve data quality of multi-researcher datasets for the analysis of morphological variation. Am. J. of Biol. Anthropol., 183, 60-78. https://doi.org/10.1002/ajpa.24836

 

Marquès Gomila, C.; Kiene, F.; Klein, A.; Kessler, S.E.; Zohdy, S.; Rakotondravony, R.; Durden, L.A.; Radespiel, U. (2023): Host-related and environmental factors influence long-term ectoparasite infestation dynamics of mouse lemurs in northwestern Madagascar. Am. J. Primatol., 85(6), e23494. https://doi.org/10.1002/ajp.23494

 

Springer, A.; Durden L.A.; Kiene F.; Klein, A.; Rakotondravony, R.; Ehlers, J.; Greiman, S.E.; Blanco, M.B.; Zohdy, S.; Kessler, S.E.; Strube, C.*; Radespiel, U.* (2023): Molecular phylogenetics of the sucking louse genus Lemurpediculus (Insecta: Phthiraptera), ectoparasites of lemurs, with descriptions of three new species. International Journal for Parasitology: Parasites and Wildlife, 20, 138-152. https://doi.org/10.1016/j.ijppaw.2023.02.002 (*: joint senior authors)

 

Kessler, S.; Tsangaras, K.; Rasoloharijaona, S.; Radespiel, U.; Greenwood, A.D. (2023): Long-term host-pathogen evolution of endogenous beta- and gammaretroviruses in mouse lemurs with little evidence of recent retroviral introgression. Virus Evolution, 9, 1-13. DOI: https://doi.org/10.1093/ve/veac117

Cooperation Partners:

Prof. Dr. Blanchard Randrianbinina (BR), Université de Mahajanga, Madagascar

Prof. Dr. Solofonirina Rasoloharijaona (SR), Université de Mahajanga, Madagascar

Dr. Romule Rasoloarison (RoR), Université de Mahajanga, Madagascar

Dr. Rindra Ramanankirahina (RiR), Université de Antananrivo, Madagascar

Alida Hasinianina, PhD, Madagascar

Mamy R. Evasoa, PhD, University of Mahajanga, Madagascar

Dr. L. Chikhi, Toulouse University, France and IGC, Portugal

Prof. B. Crowley, University of Cincinnati, USA

Groupe d'Étude et de Recherche sur les Primates de Madagascar

Prof. J. Ratsimbazafy, University of Antananarivo, Madagascar

Funding: BMBF, Conservation International, DFG, Operation Wallacea, Volkswagen-Stiftung, DAAD (PhD/reinvitation fellowship to BB, SR, RoR, AR RiR, AH) as well as to supervisors, Small Rufford Fund, private organisations

Project Details:
The Ankarafantsika National Park and the Mariarano forest contain different habitat types, including xerophytic forests, dry deciduous forests, semi-humid gallery forests along rivers or lake shores, coastal mangrove forests (Mariarano) and secondary vegetation formations that may develop after bushfires or selective wood extraction. This mosaic of habitat types offers many different ecological niches for lemurs and other forest dwelling organisms. Both forests are unique in northwestern Madagascar by harboring five endangered or critically endangered lemur species, one of which, the golden brown mouse lemur (Microcebus ravelobensis) was only recently described by our group in 1998. Moreover, the Ankarafantsika National Park comprises the largest remaining continuous patch of dry deciduous forest in northwestern Madagascar and is therefore of utmost importance for the longterm preservation of biodiversity in this biogeographic zone. Knowledge on the environmental flexibility of lemurs is still in its infancy, but urgently needed for conservation management. The aim of this longterm programme is to study the conservation biology of these lemur species, including their vulnerability towards diseases, at sites, for which we already have basic data. This knowledge will help to understand the environmental flexibility of species, how macrogeographic events such as climate change affect lemur?s life history and long-term survival and provide empirical data for long-term conservation management of lemurs in northwestern Madagascar.

Results:

e.g.

 

Klein, A.; Radespiel, U.; Springer, A.; Rakotondravony, R.; Strube, C. (2024): Temporal dynamics in gastrointestinal helminth infections of sympatric mouse lemur species (Microcebus murinus and Microcebus ravelobensis) in Northwestern Madagascar. International Journal for Parasitology: Parasites and Wildlife, 25, 100972. https://doi.org/10.1016/j.ijppaw.2024.100972.

 

Rasoloharijaona, S.; Randrianambinina, B.; Radespiel, U. (2024): Evidence for female dominance in the Milne-Edwards? Sportive lemur (Lepilemur edwardsi). American Journal of Primatology, e23658. https://doi.org/10.1002/ajp.23658.

 

Steffens, T.S.; Ramsay, M.S.; Andriatsitohaina, B.; Cosby, A.E.; Lehman, S.M.; Rakotondravony, R.; Razafitsalama, M.; Teixeira, H.; Radespiel, U. (2022): Shifting biogeographic patterns of Microcebus ravelobensis and M. murinus. Int. J. Prim., 43, 636-656. https://doi.org/10.1007/s10764-022-00304-z.

 

Wuesthoff, E.; Fuller T.K.; Sutherland, C.; Kamilar, J.M.; Ramanankirahina, R.; Rakotondravony, R.; Rouse, S.; Radespiel, U. (2021): Spatial partitioning of sympatric species of mouse lemurs across a mangrove-dry forest habitat gradient. J. Mammal. 102(5), 1266-1278. https://doi.org/10.1093/jmammal/gyab082.

 

Durden, L.A.; Kessler, S.E.; Radespiel, U.; Hasiniaina, A.F.; Stekolnikov, A.A.; Chalkowski, K.; Zohdy, S. (2021): Host associations of ectoparasites of the gray mouse lemur, Microcebus murinus, in northwestern Madagascar. J. of Parasitol. 107(1), 108-114. https://doi.org/10.1645/20-145.

Cooperation Partners:

Prof. Solofonirina Rasoloharijaona, University of Mahajanga, Madagascar

Prof. Blanchard Randrianambinina, University of Mahajanga, Madagascar

Dr. Romule Rakotondravony, University of Mahajanga, Madagascar

Dr. Rindra Ramanankirahina, University of Antananarivo, Madagascar

Dr. Hanta Razafindraibe, University of Antananarivo, Madagascar

Dr. Peter Long, Oxford University, U.K.

Prof. Shawn Lehman, Toronto University, Canada

Prof. Brooke Crowley, Univerisity of Cincinnati, USA

Prof. Hermann Behling, Georg-August-Universität Göttingen

Prof. Travis Steffens, University of Guelph, Canada; Planet Madagascar