Research

Project Details:
Stable and consistent individual behavioral variations in animals that are generally regarded as an expression of animal personalities, and might be important drivers of ecological specialization and the evolutionary adaptive potential of species. We aim to investigate various proximate factors driving individual variations in risk-taking behavior of the grey mouse lemur (Microcebus murinus) as well as their relationship and explanatory value for physical cognitive performance. In the wild, this species lives under a very high predation pressure and risk taking decisions must therefore be taken on a daily basis and should be an important key to survival. We will study captive grey mouse lemurs with a longitudinal approach to investigate systematically the individual behavioral dynamics across time and different risk contexts. In a second step, personality differences will then be compared with the results from a test battery in the physical cognitive domain. Our findings will contribute to a better understanding of risk taking as one facet of animal personality in one of the world’s smallest primates.

Results:

Splinter, F.; Fichtel, C.; Radespiel, U. (2025): Wild and captive Grey Mouse Lemurs (Microcebus murinus) differ in cognitive performance. Int. J. Prim., 46, 644-663. https://doi.org/10.1007/s10764-025-00490-6

Project Details:
Mouse lemurs are the smallest primates on earth. They are endemic to Madagascar, where they are increasingly endangered by anthropogenically caused habitat degradation. Mouse lemurs are unique primate models for evolutionary, aging and genomic research. They exhibit extraordinary species diversity with limited vs. broad ranges in the Malagasy tropical forests. They have a long longevity related to body size (up to 15 years in the laboratory, about 9 years in the field) which is, however, much shorter than for common anthropoid primate models. Furthermore, some, but not all, aging individuals develop an AD-like pathology as found in Alzheimer patients or show human-like aging-related diseases such as cancer or ocular pathologies (e.g. cataracts). Likewise mouse lemurs are one of the primate models, for which the full genome is published. In 1985, Elke Zimmermann founded the colony of gray mouse lemurs of the Institute of Zoology (IfZ), by two founder pairs coming from the University of Tübingen (Jörg Ganzhorn). Founder pairs stem from the Rotterdam Zoo and were tracked back to their origin in south-eastern Madagascar (Mandena). To increase the genetic diversity of the colony, the offspring of these founders (originally based at the University of Stuttgart-Hohenheim, moving later on to the University of Constance, the German Primate Centre and finally completely to the Institute of Zoology at the University of Veterinary Medicine in Hannover) were cross-bred with mouse lemurs coming from the Rotterdam Zoo, the Netherlands, in 1993 and the Parc Zoologique de Vincennes, France, in 1996. The colony is a self-sustaining breeding colony for which the life history of each individual mouse lemur is documented from birth to death in a mouse lemur database. Tissues from these individually known mouse lemurs are collected for veterinary purposes, or after the natural death of an animal. This colony of mouse lemurs is registered in the European and International Studbook of the Cheirogaleidae. Animals are used for non-invasive integrative and comparative research in the field of behaviour, physiology, reproduction, sensory biology, communication, cognition, genetics/genomics, aging, conservation biology and veterinary medicine. Furthermore, they are used for comparative research projects that are conducted together with several academic institutions studying the effect of different factors (e.g. general maintenance conditions, different photoperiod regimes, enrichment, group composition, genetic lineages) on the physiology, behaviour, communication, cognition, reproduction, longevity and health status of the colonies.

Results:

e.g.

The Tabula Microcebus Consortium*; Ezran, C.; Liu, S.; Chang, S.; Ming, J.; Botvinnik, O.; Penland, L.; Tarashansky, A.; de Morree, A.; Travaglini, K.J.; Zhao, J.; Wang, G.; Hasegawa, K.; Sin, H.; Sit, R.; Okamoto, J.; Sinha, R.; Zhang, Y.; Karanewsky, C.J.; Pendleton, J.L.; Morri, M.; Perret, M.; Aujard, F.; Stryer, L.; Artandi, S.; Fuller, M.; Weissman, I.L.; Rando, T.A.; Ferrell Jr., J.E.; Wang, B.; De Vlaminck, I.; Yang, C.; Casey, K.M.; Albertelli, M.A.; Pisco, A.O.; Karkanias, J.; Neff, N.; Wu, A.R.; Quake, S.R.; Krasnow, M.A. (2025): Tabula Microcebus: A molecular cell atlas of mouse lemur, an emerging model primate. Nature, 644:173-184. https://doi.org/10.1038/s41586-025-09113-9. (* U.R. member of the Microcebus Consortium)

 

Ezran, C.; Liu, S.; Chang, S.; Ming, J.; Guethlein, L.A.; Wang, M.F.Z.; Dehghannasiri, R.; Olivieri, J.; Frank, H.K.; Tarashansky, A.; Koh, W.; Jing, Q.; Botvinnik, O.; Antony, J.; The Tabula Microcebus Consortium*; Oliveira Pisco, A.; Karkanias, J.; Yang, C.; Ferrell Jr., J.E.; Boyd, S.D.; Parham, P.; Long, J.Z.; Wang, B.; Salzman, J.; De Vlaminck, I.; Wu, A.; Quake, S.R.; Krasnow, M.A. (2025): Mouse lemur cell atlas informs primate genes, physiology, and disease. Mouse lemur cell atlas informs primate genes, physiology and disease. Nature, 644: 185-196. https://doi.org/10.1038/s41586-025-09114-8. (* U.R. member of the Microcebus Consortium)

 

Wittkowski, J.*; Klein, A.*; Kollikowski, A.*; Scheumann, M.*; Schmidtke, D.*; Zimmermann, E.†*; Radespiel, U.* (2024): The mouse lemurs. In: The UFAW Handbook on the Care and Management of Laboratory and Other Research Animals, 9th Edition. (H. Golledge, C. Richardson, eds.). John Wiley & Sons Ltd. (*: contributed equally to this chapter), pp. 662-682. https://doi.org/10.1002/9781119555278.ch36.

 

Bleyer, M.; Radespiel, U.; Klein, A.; Kollikowski, A.; Ströbel, P.; Mätz-Rensing, K.; Gruber-Dujardin, E. (2024): Spontaneous soft tissue tumours in aged mouse lemurs. Journal of Comparative Pathology, 215, 47-54.

 

Fritz, R.; Zimmermann, E.; Meier, M.; Mestre-Francés, N.; Radespiel, U.; Schmidtke, D. (2020): Neurobiological substrates of animal personality and cognition in a nonhuman primate (Microcebus murinus). Brain and Behavior, e01752. https://doi.org/10.1002/brb3.1752.

Cooperation Partners:

Prof. Pees, Klinik für Heimtiere

Zoo Zürich, Schweiz; Zoo Frankfurt, Zoo Landau,

Zoo Vincennes, Frankreich; Zoo Pilsen, CZ

Prof. J.-M. Verdier, École Pratique des Hautes Études, Paris, Frankreich

Project Details:
Aposematic warning coloration is primarily associated with deterring potential predators. However, only limited knowledge exists regarding the role of such visual signals in intraspecific communication. The aim of this study is to enhance the color intensity of a group of dorsally yellow Dendrobates tinctorius from the locality "Citronella" through dietary supplementation with carotenoids, such as β-carotene and lutein derivatives. The underlying assumption of this experiment is that coloration can be modified through carotenoid supplementation to a degree that allows supplemented individuals to be distinguished from unsupplemented ones by the naked eye, as well as through measurable shifts in reflectance spectra. Individuals exhibiting different levels of pigmentation (supplemented and supplemented = control) will be put together in a test arena for mate-choice experiments and the assessment of territorial behavior. There is reason to assume that particularly intense coloration confers selective advantages in terms of mate choice or dominance behavior, as has been suggested in previous studies on strawberry poison frogs. Such selective advantages, including increased attractiveness or greater competitive ability, are of particular interest in the context of the evolutionary mechanisms underlying warning coloration and the pronounced phenotypic variation observed among different local populations. The study will examine whether the color differences are perceptible to the frogs themselves and how individuals from the two experimental groups respond behaviorally to differently colored conspecifics. Previous studies further suggest that carotenoids may have a stimulatory effect on clutch production. To test this assumption, the reproductive performance of the separately housed experimental groups will be analyzed. The insights gained from this work may contribute to improved amphibian husbandry, provide new perspectives on intraspecific communication, and shed light on the mechanisms driving the evolution of aposematic coloration.

Project Details:
The monitoring and evaluation of emotions in animals is of increasing interest due to the public awareness on anima, welfare but also because laboratory animals serve as model species for the development of psychological drugs. The reliable evaluation of emotions is still a scientific challenge, as emotions are not only the result of automatic physiological reactions, but also underline cognitive evaluation processes (Kalat & Shiota, 2007). Thus, the emotional perception of a situation can depend on individual personality or experience. In order to be able to assess animal welfare, it is important to develop reliable methods for recording the emotional state of an animal. Although it is possible to determine an animal's condition using physiological measurements (e.g. blood sampling, implants to measure the heart rate), these measures are invasive and do not provide any information about the emotional valence of the condition (an increased heart rate occurs with both negative and positive emotions). An alternative is offered by behavioural tests that can be used to test the personality of animals as well as the emotional cognitive evaluation of a situation. One way of testing cognitive judgement is the ‘Judgement Bias Task’. The animal learns to distinguish between a positive and a less positive stimulus and to react accordingly. They are then presented with an unknown ambivalent stimulus. Their reaction makes it possible to assess whether an animal is ‘optimistic’ (selects as with a positive stimulus) or ‘pessimistic’ (selects as with a positive stimulus). These findings will allow a better assessment of emotions in animals and can later be used to investigate the impact of different housing conditions, environmental enrichment or pharmacological effects on an animal's emotions.

Funding: DBU, CULT-Stiftung, 81.550 EUR

Project Details:
This project serves the long-term purpose of protecting the species of the yellow-bellied toad, Bombina variegata, which is highly endangered in Germany and Central Europe. In many areas, the yellow-bellied toad only occurs in secondary, i.e. anthropogenically modified, habitats such as quarries. The populations are often isolated, too small, and suffer from inbreeding and genetic impoverishment. Previous studies have also shown that yellow-bellied toads use different life cycle strategies in different habitats. These differences suggest that the species has adapted to local ecological conditions, and these adaptations are potentially manifested in the genome. The project aims to improve the genetic and ecological information available about the species in order to make practical conservation more effective. For this purpose, DNA samples from German, French and Swiss yellow-bellied toad populations, which have already been sampled in previous projects, are examined using genomic methods (RADSeq). In addition, toads in Germany will be sampled in the few natural habitats where they still occur. The genomic results are then correlated with ecological data (habitat type, local climate). The results provide evidence as to whether yellow-bellied toads are adapted to their local habitat (anthropogenic vs. natural) or to their local climate at the molecular level. The aim is to identify specific candidate genes that mediate this local adaptation. Furthermore, species distribution models based on climatic data should show where suitable habitats are for the yellow-bellied toad today and in the future - also with a view on climate change. The results obtained will be discussed with scientists and species protection specialists in a workshop. In follow-up projects, so-called genetic rescue will be used for small, isolated occurrences to stabilize them, and larger populations will be genetically upgraded. Genetic rescue projects based on genomic information are innovative since so far they have been successfully implemented in species protection in only a few countries.

Cooperation Partners:

Prof. Jean-Paul Léna, Dr. Hugo Cayuela, Benjamin Monod-Broca, University of Lyon;

Dr. Mirjam Nadjafzadeh, NABU Niedersachsen; Fabian Droppelmann, Chance 7

Funding: DAAD, 24.705 EUR

Project Details:
Aposematism and crypsis are contrasting antipredator strategies. In the color polymorphic Oophaga pumilio, phylogenetic analyses have shown that populations with cryptic and aposematic coloration might have evolved independently in different islands. Two other species, O. granulifera and O. vicentei also display cryptic and aposematic color morphs in geographically isolated populations. Particularly, phylogenetic analyses of the evolution of these contrasting antipredator strategies can improve our understanding on the evolution of polymorphism in aposematic species. This project aims to uncover the molecular signatures of selection present in the genes of three Oophaga species that experienced independently evolved cryptic and aposematic phenotypes. To this effect, we look forward to elucidate the phylogenetic relationships of the genus and quantify the variation in gene expression and allelic frequencies using state-of-the-art methods.

Results:

Cajigas Gandia A, Rodríguez A, Mantzana Oikonomaki V, Pröhl H (2024) Genomic signatures of selection for aposematism and crypsis in Oophaga poison frogs. Poster. EMBO Early Career Lecture Course "Evolutionary and Comparative Genomics" Nafplion, Greece

Cooperation Partners:

Dr. Evan Towney, Goethe Universität Frankfurt, Biologicum

Project Details:
With Alexa, Siri and Cortana, voice recognition and control software has become an integral part of our everyday lives. Animal voices also contain a huge number of information about the sender animal, such as species, identity, gender, age, body size, emotional state, diseases and hormone status. Bioacoustics therefore enables the development of non-invasive, time- and cost-efficient, automatic bioacoustic monitoring systems for animals. For this purpose, microphones can be installed recording animals' vocalisations around the clock without disturbing or influencing them. The recordings can be automatically analysed using mathematical algorithms to extract specific information. In addition, psychoacoustic tools can be used to elicit specific positive behaviours. Such bioacoustic tools can be used for clarification of taxonomic questions, to monitor wildlife as well as to improve animal husbandry and thus play an increasingly important role in species conservation and animal management. The aim of this project is to explore the wide range of possible applications and to develop bioacoustic monitoring systems for species conservation and animal management.

Results:

van Elst T, Sgarlata GM, Schüßler D, Tiley GP, Poelstra JW, Scheumann M, Blanco MB, Aleixo-Pais IG, Rina Evasoa M, Ganzhorn JU, Goodman SM, Hasiniaina AF, Hending D, Hohenlohe PA, Ibouroi MT, Iribar A, Jan F, Kappeler PM, Le Pors B, Manzi S, Olivieri G, Rakotonanahary AN, Rakotondranary SJ, Rakotondravony R, Ralison JM, Ranaivoarisoa JF, Randrianambinina B, Rasoloarison RM, Rasoloharijaona S, Rasolondraibe E, Teixeira H, Zaonarivelo JR, Louis EE, Yoder AD, Chikhi L, Radespiel U, Salmona J (2025). Integrative taxonomy clarifies the evolution of a cryptic primate clade. Nature Ecology & Evolution, 9(1), 57-72. DOI:10.1038/s41559-024-02547-w.

 

Heseker P, Bergmann T, Liebolt M-A, Traulsen I, Kemper N, Probst J, Scheumann M (2024a). Exposing tail biters by automatic scream detection. Smart Agricultural Technology, 9. DOI:10.1016/j.atech.2024.100582.

 

Heseker P, Bergmann T, Scheumann M, Traulsen I, Kemper N, Probst J (2024b). Detecting tail biters by monitoring pig screams in weaning pigs. Scientific Report, 14(1), 4523. DOI:10.1038/s41598-024-55336-7.

 

Pfannerstill V, Balkenhol N, Bennitt E, Maboga O, Scheumann M (2023a). Assessing the potential of conspecific playbacks as a post-translocation management tool for white rhinoceros. Conservation Science and Practice, 5(9), e12996. DOI:10.1111/csp2.12996.

 

Hasiniaina AF, Radespiel U, Kessler SE, Evasoa MR, Rasoloharijaona S, Randrianambinina B, Zimmermann E+, Schmidt S, Scheumann M+ (2020). Evolutionary significance of the variation in acoustic communication of a cryptic nocturnal primate radiation (Microcebus spp.). Ecology and Evolution, 10(8), 3784-3797. DOI:10.1002/ece3.6177; + shared senior authorship

Project Details:
Oophaga pumilio, better known as the strawberry frog, belongs to the family of poison dart frogs (Dendrobatidae). These tiny tropical frogs are immediately recognizable by their intense coloration. Within the species O. pumilio, there is pronounced color polymorphism, expressed in a wide range of skin colors and patterns. Cryptic individuals usually have a green, inconspicuous coloration, while aposematic individuals are characterized by bright colors ranging from intense red to brilliant yellow. The color intensity of O. pumilio thus plays a central role in predator defense, and further studies have shown different colors to play a role in mate selection. It is also known that the color receptors in the retina enable the frogs to distinguish between the color morphs and that carotenoid pigments play a central role in the expression of coloration. Carotenoids are fat-soluble pigments that are responsible for pink, red, orange, and yellow coloration. Since O. pumilio cannot produce carotenoids itself, it must obtain them from animal prey. After ingestion, the carotenoids are absorbed in the gastrointestinal tract, metabolized, and then stored in the skin and other organs, such as the eyes. As part of a feeding experiment, the frogs will be supplemented with carotenoids to determine the influence of these pigments on skin coloration and to gain a better understanding of color development in O. pumilio.
The natural range of O. pumilio includes western Panama, the Caribbean coast of Costa Rica, and parts of Nicaragua. The species inhabits tropical rainforests with dense vegetation and is often observed at forest edges near the coast. Given their average body weight of around half a gram, the question remains as to how these small animals orient themselves in the complex structures of dense rainforests in their territories of several square meters. To answer this question, two independent behavioral experiments will be conducted to investigate the spatial learning behavior of Oophaga pumilio using visual signals that differ in coloration.

Funding: Madagascar National Parks; Kölner Zoo, 132.620 EUR

Project Details:
The overall objective of this project is to understand the effects of forest fires on vegetation and wildlife dynamics in dry deciduous forests of western Madagascar and to model their long-term post-fire regeneration potential by applying a landscape approach. This study will build on the fire history of the last 35 years within Ankarafantsika National Park (ANP) derived from annually available remote sensing data. We aim to investigate the impact of different time spans since the last fire, fire severity and different fire intervals on forest integrity on the one hand, and on lemur population dynamics as one representative and enigmatic, forest-dependent, vertebrate group on the other hand. Lemurs are highly suitable study species in this respect, since they fulfill key ecosystem functions (e.g. pollination, seed dispersal, food-web interactions), and the presence of the complete lemur assemblage indicates intact forest habitats. This will allow a prognosis of the long-term regeneration potential of recently burnt areas. As such, this project will provide guidance for a sustainable conservation management in the region and beyond, and will help to identify preferable areas for forest restoration and therefore nature-based-solutions towards pressing environmental problems in Western Madagascar.

Results:

Rabemananjara, N.R.; Rasolozaka, M.M.; Ravolanirina, M.O.; Marivola, R.; Randriamiarantsoa, S.H.; Rakotondravony, R.; Razafindraibe, H.; Schüßler, D.; Radespiel, U. (2025): Post-fire recolonization of dry deciduous forests by lemurs in northwestern Madagascar. Biodiv. Cons. 34, 4545-4574. https://doi.org/10.1007/s10531-025-03167-x

 

Rasolozaka, M.; Schüßler, D.; Randriafenontsoa, J.; Andriatsitohaina, F.; Rakotomamonjy, P.; Rabarison, H.; Radespiel, U. (2025): Reconstructing the alarming fire history of Ankarafantsika National Park in northwestern Madagascar over a 35 year-period. Remote Sensing Applications: Conservation and Society, 33, 101521. https://doi.org/10.1016/j.rsase.2025.101521

Cooperation Partners:

Dr. Harison Rabarison, University of Antananarivo, Madagascar

Dr. Hanta Razafindraibe, University of Antananarivo, Madagascar

Dr. Romule Rakotondravony, Universitity of Mahajanga, Madagascar

Dominik Schüßler, MSc, Universität Hildesheim

Funding: DFG, 242.660 EUR

Project Details:
Aposematism is the association between a bright warning colouration and a defence mechanism, (e.g. toxins) for avoiding predation. The genetics of colouration and toxicity in aposematic animals is still not well investigated. In this context, the diversity of alkaloids in the skin and colouration patterns linked to predator avoidance strategies in Neotropical poison frogs is an exciting opportunity to study the convergence of ecological adaptation. Poison frogs differ in colouration patterns and toxicity among populations and strong evidence exists that aposematism is adaptive, probably driven by predator selection. For the strawberry frog Oophaga pumilio, we were able to show that genes related to pigment metabolism (e.g. pteridinene) are differently expressed between color morphs. The next objective is to connect the structure of cells containing pigment (chromatophores), the chromatographic characterization of color pigments and alkaloids, expression patterns of genes that are involved in coloration and toxicity for three color-polymorphic, neotropical poison dart frogs of the genus Oophaga.

For our project, we will collect skin and liver samples from eight populations with either green or red colouration in Panama and Costa Rica. Together with collaborators from the University of Costa Rica, the TiHo, the University of Cambridge and STRI in Panama we will characterize the chromatophores in the skin by electron microscopy, analyse the colour pigments and toxins in the skin by gas chromatography, and will perform RNAseq analysis on dorsal skin-derived cDNA. We expect that expression levels of genes in pigment (e.g. carotenoid pathways) and alkaloid metabolism to vary among different colour morphs (red vs. green) but to be similar within colour morphs across species due to convergence. Our study will lead to a better understanding of the link between geno- and phenotypes of adaptive anti-predator strategies and illuminate the evolution of regulatory mechanisms of gene expression.

Results:

Kehrt LF, Vasquez V, Mora-Machado A, Mantzana-Oikonomaki V, Ibáñez R, Rodriguez A, Pröhl H, Tamayo-Castillo G. Alkaloid profiles in red and green color morphs of Neotropical poison frogs: untangling aposematic strategies in Oophaga granulifera and O. pumilio. Scientific Reports (in revision).

 

Mantzana-Oikonomaki V, Tamayo-Castillo G, Zamora Ramirez WJ, Ibáñez R, Pröhl H, Ariel Rodríguez A (2025) Gene expression and histological differences drive color divergence in the Panamanian poison frog Oophaga vicentei. Molecular Ecology 35: e70214. doi.org/10.1111/ mec.70214

 

Méndez-Rivera M, Ramírez-Morales D, Mora-Machado A, Pröhl H, Rodríguez A, Okada T, Toyooka N, Ibáñez R, Rodríguez-Rodríguez CE, Tamayo-Castillo G (2025) Acute toxicity of skin-homologues synthethic alkaloids and frog-skin extracts: miniaturized test to evaluate toxicity with Daphnia magna. Toxicon 268: 108599. doi.org/10.1016/j.toxicon.2025.108599

 

Mantzana-Oikonomaki V, Rodríguez A, Castillo-Tamayo G, Ibáñez R, Pröhl H (2024) Predator perception of aposematic and cryptic color morphs in two Oophaga species. Ecology and Evolution, 14: e70351. https://doi.org/10.1002/ece3.70351

 

Monteiro JPC, Ibáñez R, Mantzana-Oikonomaki V, Pröhl H, Rodríguez A (2023) Genetic diversity of Oophaga vincentei (Anura: Dendrobatidae) and taxonomic position of a remarkable color morph from Panama. Salamandra 59: 347-351

Cooperation Partners:

Dr. Giselle Tamayo, UCR, Costa Rica

Dr. Beatriz Willink, UCR, Costa Rica

Dr. Nicolas Mundy, University of Cambridge, UK

Dr. Roberto Ibañéz, STRI, Panama