Research

      Main current projects
      Updated in August 2020


Species and range evolution in Amazonian amphibians
Since 2002.
It is challenging to explain amphibian history and diversity in Amazonia. Our molecular-, field- and model-based research on amphibians contributes towards a better understanding of the role of e.g. the various modes of dispersal or how secondary contact contributes to evolutionary change within or between species. A particular research focus are on 'floating meadows' on the Amazon river and its tributaries.
Taxonomic key groups are poison frogs (Dendrobatoidea) and harlequin toads (Atelopus).

Key publications:
Marin da Fonte, L.F., M. Mayer & S. Lötters (2019): Review: Long-distance dispersal in amphibians. — Frontiers in Biogeography, 11.4: e44577.
[online]
Mayer, M. et al. (2019): Mind the gap! A review of Amazonian anurans in GenBank. — Salamandra, 55: 89-96.
Gehara, M. et al. (2014): High levels of diversity uncovered in a widespread nominal taxon: continental phylogeography of the Neotropical tree frog Dendropsophus minutus. — PLoS ONE, 9: e103958. [online]
Lötters, S. et al. (2010): Reinforcing and expanding the predictions of the disturbance vicariance hypothesis in Amazonian harlequin frogs: a molecular phylogenetic and climate envelope modelling approach. — Biodiversity and Conservation, 19: 2125-2146.
[online]

Photo: Ameerega trivittata, a fellow found over most of Amazonia. By Denise J. Ellwein.

Functional aspects and evolution of aposematism
in brilliant-colored and not so colorful toxic toads

Since 2012.
Harlequin toads (Atelopus) greatly vary between cryptic and brilliant colorations and some just have flashing red hand and foot soles. All Atelopus are toxic. They contain tetrodotoxin (TTX) which is puzzling, as this highly venomous substance is, other than in amphibians, known from many marine organisms (including puffer fish, a delicacy in Japan). We study the evolution and function of visual conspicuousness with regard to toxicity. Part of our field experiments use differently colored clay models of toads. 

Key publications:
Rößler, D.C. et al. (2019): Sole coloration as an unusual aposematic signal in a Neotropical toad. — Scientific Reports, 9: 1128. [online]
Mebs, D., M. Lorentz, M. Yotsu-Yamashita, D.C. Rößler, R. Ernst & S. Lötters (2018): Geographic range expansion of tetrodotoxin in amphibians – first record in Atelopus hoogmoedi from the Guiana Shield. — Toxicon, 150: 175-179.
Lorentz, M.N. et al. (2016): Tetrodotoxin in animals. — Current Biology, 26: R870-R872.
Lötters, S. et al. (2011): Assessing the molecular phylogeny of a near extinct group of vertebrates: the Neotropical harlequin frogs (Bufonidae; Atelopus). — Systematics and Biodiversity, 9: 45-57.

Photo: An undescribed toxic Atelopus species from Ecuador. By Jos Kielgast.

Predator-prey relationships inferred from attacks on artifical prey
Since 2016.
Predator-prey interactions are a vast field in ecological research and many mechanisms thereof are crucial to understand natural selection, trait functions, cognition of traits and hence their evolution. However, for many taxa predator-prey interactions are difficult to study because field observations of predation events are rare. Predation is based on perception of stimuli, in many cases visual cues.
To understand the effects of different visual cues on predation, such as coloration or patterns of prey animals, we use artificial prey to collect information. We mainly work with European land salamanders but have also collected data on Neotropical harlequin toads (see above). In a recent study we were able to demonstrate that potential predators leave DNA on clay models that helps identfying them.

Key publications:
Rößler, D.C. et al. (2018): Commentary: the future of clay model studies. — BMC Zoology, 3: 6. [online]
Rößler, D.C. et al. (2020): An amplicon sequencing protocol for attacker identification from DNA traces left on artificial prey. — Methods in Ecology & Evolution, in press
[online]

Photo: A 'battery' of fire salamander clay models ready to be place in the field. By Stefan Lötters.

How do emerging infectious diseases affect amphibian diversity?
Special focus: The salamander-eating fungus 'Bsal' in Western Europe
Since 2008.
Emerging infectious diseases are one of the main threats to global biodiversity. Amphibians, a group severely declining at the global scale, suffer from spreading fungal diseases, in particular the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd). We have studied this pathogen in the wild in the Alps and in East Africa and have made a risk assessment for all global amphibian species, based on distribution models.
Some years ago, a new amphibian skin fungus, Batrachochytrium salamandrivorans (Bsal), was discovered in western Europe. It is lethal to many salamander and newt species (not so to frogs and toads or caecilians, as far as we know), and our native amphibian fauna is at high risk of extinction. Our studies mainly focus on how the new fungus, which might have originated in Asia (where asymptomatic species have been found), spreads and how it affects populations in the wild. In 2015, we have recorded it for the first time in Germany (see below: Spitzen-van der Sluijs et al. 2016). For some years now we have witnessed a significant spread of Bsal in parts of Germany along with dramatic declines in fire salamander (Salamandra salamandra) populations. Newts are also affected in the wild but apparently can cope better with the fungus. An exception might be the norther crested newt (Triturus cristatus), but further research is needed.
For more information see a film made by students from Trier University. The recent knowledge on Bsal in Germany was summarized in a thematic issue of SALAMANDRA, published 15 August 2020.

Key publications: 
Lötters, S. et al. (2020): The amphibian pathogen Batrachochytrium salamandrivorans in the hotspot of its European invasive range: past - present - future. — Salamandra, 56: 173-188. [online]
Lötters, S. et al.  (2020): Bsal-driven salamander mortality pre-dates the European index outbreak. — Salamandra, 56: 239-242.
[online]
Lötters, S. et al. (2018): First report of host co-infection of parasitic amphibian chytrid fungi. — Salamandra, 54: 287-290.
[online]
Canessa, S. et al. (2018): Decision making for mitigating emerging wildlife diseases: from theory to practice. — Journal of Applied Ecology, 55: 1987-1996.

Martel, A. et al. (2014): Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. — Science, 346: 630-631
[online]
Lötters, S. et al. (2012): Absence of infection with the amphibian chytrid fungus in the terrestrial Alpine salamander, Salamandra atra. — Salamandra, 48: 58-62
.
Rödder, D. et al. (2009): Global amphibian extinction risk assessment for the panzootic chytrid fungus. — Diversity, 1: 52-66.[online]

Photo: Fire salamander (Salamandra salamandra):
Still common, but soon severly threatened? By SIVAE.

Right hand side is a global model of the potential
distribution of the amphibian chytrid fungus Bd.
Warmer colors suggest higher suitability to the
pathogen and therefore higher risk to amphibians.

  Main past projects

Evolution and systematics of Afrotropical reed frogs
2003-2019.
Hyperoliid frogs comprise several hundred species with exclusively sub-Saharan African and Madagascan distributions. These so called Reed frogs are highly sexually dichromatic. Using ancestral character reconstructions on phylogenies, we found that this trait has independently developed multiple times even within one genus. In the course of the on-going research, we intend to contribute to a more complete picture of (i) the phlogeny and taxonomy and (ii) trait evolution in these mainly arboricol frogs. This generally gives some insight how plesimorphic, synapomorphic and convergent adaptations evolve within large clades.

Key publications:
Portik, D.M. et al. (2019): Sexual dichromatism drives diversification within a major radiation of African amphibians. — Systematic Biology, 6: 859-875.
Bell, R.C. et al. (2017): Idiosyncratic responses to climate-driven forest fragmentation and marine incursions in reed frogs from Central Africa and the Gulf of Guinea Islands. — Molecular Ecology, 26: 5223-5244.
Channing, A. et al.(2013): Taxonomy of the super-cryptic Hyperolius nasutus group of long reed frogs of Africa (Anura: Hyperoliidae), with descriptions of six new species. — Zootaxa, 3620: 301-350.
Schick, S., et al. (2010): New species of reed frog from the Congo basin with discussion of paraphyly in Cinnamon-belly reed frogs. — Zootaxa, 2501: 23-36.
Veith, M. et al. (2009): Multiple evolution of sexual dichromatism in African reed frogs. — Molecular Phylogenetics and Evolution, 51: 388-393.

Photos: Sexual dichromatism in Hyperolius viridiflavus from Kenya: females are green-yellow, males have the same color or are brownish. By Stefan Lötters.

Species, time and space — Biogeography of the Congo Basin
2004-2017.
Africa's 'green heart' is among the least explored rainforests, remarkably huge in size. We are interested in understanding past and on-going distributional patterns and processes. Our key groups comprise anurans. Apart from the collection of basics (including the description of new species), we study dispersal, vicariance and identify potential refuges, making use of molecular phylogenetic data as well as species distribution models.

Key publications: 
Bell, R.C. et al. (2017): Idiosyncratic responses to climate-driven forest fragmentation and marine incursions in reed frogs from Central Africa and the Gulf of Guinea Islands. — Molecular Ecology, 26: 5223-5244.
Zimkus, B.M. et al. (2017): Leapfrogging into new territory: How Mascarene ridged frogs diversified across Africa and Madagascar to maintain their ecological niche. — Molecular Phylogenetics and Evolution, 106: 254-269.
Bell, R.C. et al. (2015): Over-seas dispersal of Hyperolius reedfrogs from Central Africa to the oceanic islands of São Tomé and Príncipe. — Journal of Biogeography, 42: 65-75.

Photo: Beautiful rainforests in DRC. By Jos Kielgast.

Intra- and interspecific signalling in poison frogs
2009-2014.
This species lays eggs on land and transports its larvae singly into water pools in leaf axils (phytotelms). We found that nurse frogs do avoid pools occupied by conspecific tadpoels on the basis of chemical recognition. Phytotelms do provide limited resources only and tadpoles are cannibalistic. We have been able to show that sometimes tadpoels of other frog species are avoided, too (e.g. Hyloxalus azureiventris), but that occasionally pools with (chemical compounds of) tadpoles of heterospecifics are 'preferred'. The latter especially applies to non-cannibalistic tadpoles (e.g. Rhinella poeppigii). Interestingly, nurse frogs are unable to detect insect predators in phytotelms on the basis on chemical compounds.
Combining chemical analyses with in-situ bioassays, we identified the molecular formulas of the chemical compounds triggering the nurse frog's behavior. Ranitomeya variabilis and Hyloxalus azureiventris both produce distinct chemical compound combinations. This leads us to conclude that two separate communication systems are at work. In an ecological context, we classify the conspecific R. variabilis compounds as chemical cues - that is, they are only advantageous to the receiver (nurse frog), not the emitters (tadpoles). The heterospecific compounds, we suggest are chemical signals. These are advantageous to the emitters (heterospecific tadpoles) and likely also to the receivers (nurse frog). Due to these assumed receiver benefits, the heterospecific compounds are possibly synomones which are advantageous to both emitter and receiver. This would be a very rare communication system between animal species, especially vertebrates. 

Key publications:
Schulte, L.M., M. Krauss, S. Lötters, T. Schulze & W. Brack (2015): Decoding and discrimination of chemical cues and signals: Avoidance of predation and competition during parental care behavior in sympatric poison frogs.
— PLoS ONE, 10: e0129929. [online
Schulte, L.M. & S. Lötters (2013): The power of the seasons: rainfall triggers parental care in poison frogs. — Evolutionary Ecology, 27: 711-723.
Schulte, L.M. et al. (2011): The smell of success: choice : choice of larval rearing sites by means of chemical cues in a Peruvian poison frog. — Animal Behaviour, 81: 1147-1154.

Photo: Male Ranitomeya variabilis carrying a tadpole on its back. By Lisa M. Schulte.

Contact zones in the parapatric Alpine and Fire salamanders
2010-2014.
Parapatric species which meet in small contact zones pose interesting questions. With the aim to to identify the determinants
for contact zones in these two land salamanders, our research combines (i) new methodical approaches in ecological modelling at various spatial scales and (ii) life history field studies.

Key publications: 
Werner, P. et al. (2017): Microhabitat use within a contact zone of parapatric land salamanders in the Swiss Alps. — Amphibia-Reptilia, 38: 307-314.
Werner, P. et al. (2014): Analysis of habitat determinants in a contact zone of parapatric European salamanders. — Journal of Zoology, 292: 31-38.
Werner, P. et al. (2013): The role of climate for the range limits of parapatric European land salamanders. — Ecography, 36: 1127-1137
.

Photo: Amazing Alpine salamander portrait. By Ulrich Schulte.

 

Modelling range shifts in Foraminifera
2009-2013.
Key publications:
Weinmann, A.E. et al. (2013):
Heading for new shores: Projecting marine distribution ranges of selected larger foraminifera. — PLoS ONE, 8: e2182. [online]
Langer, M.R. et al. (2013): Climate-driven range extension of Amphistegina (Protista, Foraminiferida): models of current and predicted future ranges. — PLoS ONE, 8: e54443. [online]
Langer, M.R. et al. (2012): “Strangers” in paradise: modeling the biogeographic range expansion of the foraminifera Amphistegina in the Mediterranean Sea. — Foraminiferal Research, 42: 234-244.

Above is shown the potential New World distribution of Amphistegina spp. under current and future climatic conditions (for the year 2050, right). Warmer colors suggest higher suitability; that is a trend to decrease with anthropogenic warming.

Effects of environmental contaminants in amphibians and reptiles
2010-2018.
Changing land use practices in agriculture may increase the contamination risk to amphibians and reptiles with pesticides. For instance, this may simply be related to the expansion of previously uncultivated areas due to the demand for energy crops, but also the cultivation of genetically manipulated crops. We investigate direct and indirect effects of environmentally (and legally) pesticide concentrations on the survival of individuals, populations and species. (i) We perform lab experiments on an amphibian standard model organism (Clawed frogs, Xenopus), with a strong focus on potential effects from glyphosate-based herbicides. (ii) Wild frogs, newts, lizards and snakes are investigated in the field. Here, we aim at studying at e.g. avoidance of differently contaminated water bodies and the detection of unusual deformation rates in larvae or individual degrees of contamination, for instance, via arthropod food sources. We also use GIS-based approaches in risk analyses.

Key publications:
Mingo, V., S. Lötters & N. Wagner (2017): The use of buccal swabs as a minimal-invasive method for detecting effects of pesticide exposure on enzymatic activity in common wall lizards. — Environmental Pollution, 220: 53-62.
Mingo, V. et al.
(2016): Risk of pesticide exposure for reptile species in the European Union. Environmental Pollution, 215: 164-169.
Lötters, S. et al. (2014): Hypothesizing if responses to climate change affect herbicide exposure risk for amphibians. — Environmental Sciences Europe, 26: 31. [online]
Wagner, N. et al. (2013): Questions concenring the potential impact of glyphosate-based herbicides on amphibians. — Environmental Toxicology and Chemistry, 32: 1688-1700.

Photo: The Wall lizard (Podarcis muralis), a reptile species common in vineyards and to which pesticide contamination is relevant. By Ulrich Schulte.