Doctor of Philosophy, University of Vienna, Behavioral biology (2015)
Master of Science (M2), Université Paris Nord, Comparative Ethology (2011)
Master of Science (M1), Ecole Normale Supérieure de Paris, Ecology and Evolution (2010)
Bachelor of Science, Université Joseph Fourier (Grenoble 1), Biology (2009)
Current Research and Scholarly Interests
I’m an experimental biologist with a passion for animal behavior, natural history, and rainforest frogs. I’m interested in how the environment shapes animal behavior and animal cognitive abilities. I primarily work with South American poison frogs because they display some of the most complex spatial and social behaviors known among amphibians, but the cognitive and sensory mechanisms underlying their behavior are poorly understood. In the field, I combine tracking with experimental manipulations of frogs and their environment to understand movement patterns, navigational abilities, and the use of spatial memory. In the lab, I study the neural basis of poison frog spatial cognition.
- Simulated chorus attracts conspecific and heterospecific Amazonian explosive breeding frogs BIOTROPICA 2020
- Calling amplitude flexibility and acoustic spacing in the territorial frog Allobates femoralis BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY 2020; 74 (6)
Reproductive behavior drives female space use in a sedentary Neotropical frog.
2020; 8: e8920
Longer-range movements of anuran amphibians such as mass migrations and habitat invasion have received a lot of attention, but fine-scale spatial behavior remains largely understudied. This gap is especially striking for species that show long-term site fidelity and display their whole behavioral repertoire in a small area. Studying fine-scale movement with conventional capture-mark-recapture techniques is difficult in inconspicuous amphibians: individuals are hard to find, repeated captures might affect their behavior and the number of data points is too low to allow a detailed interpretation of individual space use and time budgeting. In this study, we overcame these limitations by equipping females of the Brilliant-Thighed Poison Frog (Allobates femoralis) with a tag allowing frequent monitoring of their location and behavior. Neotropical poison frogs are well known for their complex behavior and diverse reproductive and parental care strategies. Although the ecology and behavior of the polygamous leaf-litter frog Allobates femoralis is well studied, little is known about the fine-scale space use of the non-territorial females who do not engage in acoustic and visual displays. We tracked 17 females for 6 to 17 days using a harmonic direction finder to provide the first precise analysis of female space use in this species. Females moved on average 1 m per hour and the fastest movement, over 20 m per hour, was related to a subsequent mating event. Traveled distances and activity patterns on days of courtship and mating differed considerably from days without reproduction. Frogs moved more on days with lower temperature and more precipitation, but mating seemed to be the main trigger for female movement. We observed 21 courtships of 12 tagged females. For seven females, we observed two consecutive mating events. Estimated home ranges after 14 days varied considerably between individuals and courtship and mating associated space use made up for 30% of the home range. Allobates femoralis females spent large parts of their time in one to three small centers of use. Females did not adjust their time or space use to the density of males in their surroundings and did not show wide-ranging exploratory behavior. Our study demonstrates how tracking combined with detailed behavioral observations can reveal the patterns and drivers of fine-scale spatial behavior in sedentary species.
View details for DOI 10.7717/peerj.8920
View details for PubMedID 32337103
- Spatio-Temporal Characteristics of the Prolonged Courtship in Brilliant-Thighed Poison Frogs, Allobates femoralis HERPETOLOGICA 2019; 75 (4): 268–79
From habitat use to social behavior: natural history of a voiceless poison frog, Dendrobates tinctorius
2019; 7: e7648
Descriptive studies of natural history have always been a source of knowledge on which experimental work and scientific progress rely. Poison frogs are a well-studied group of small Neotropical frogs with diverse parental behaviors, distinct calls, and bright colors that warn predators about their toxicity; and a showcase of advances in fundamental biology through natural history observations. The dyeing poison frog, Dendrobates tinctorius, is emblematic of the Guianas region, widespread in the pet trade, and increasingly popular in research. This species shows several unusual behaviors, such as the lack of advertisement calls and the aggregation around tree-fall gaps, which remain poorly described and understood. Here, we summarize our observations from a natural population of D. tinctorius in French Guiana collected over various field trips between 2009 and 2017; our aim is to provide groundwork for future fundamental and applied research spanning parental care, animal dispersal, disease spread, habitat use in relation to color patterns, and intra-specific communication, to name a few. We report sex differences in habitat use and the striking invasion of tree-fall gaps; describe their courtship and aggressive behaviors; document egg development and tadpole transport; and discuss how the knowledge generated by this study could set the grounds for further research on the behavior, ecology, and conservation of this species.
View details for DOI 10.7717/peerj.7648
View details for Web of Science ID 000486138100005
View details for PubMedID 31576237
View details for PubMedCentralID PMC6753930
- How far do tadpoles travel in the rainforest? Parent-assisted dispersal in poison frogs EVOLUTIONARY ECOLOGY 2019; 33 (4): 613–23
- Empowering Latina scientists SCIENCE 2019; 363 (6429): 825–26
- Brilliant-thighed poison frogs do not use acoustic identity information to treat territorial neighbours as dear enemies ANIMAL BEHAVIOUR 2018; 141: 203–20
- Map-like navigation from distances exceeding routine movements in the three-striped poison frog (Ameerega trivittata) JOURNAL OF EXPERIMENTAL BIOLOGY 2018; 221 (2)
Map-like navigation from distances exceeding routine movements in the three-striped poison frog (Ameerega trivittata).
The Journal of experimental biology
2018; 221 (Pt 2)
Most animals move in dense habitats where distant landmarks are limited, but how they find their way around remains poorly understood. Poison frogs inhabit the rainforest understory, where they shuttle tadpoles from small territories to widespread pools. Recent studies revealed their excellent spatial memory and the ability to home back from several hundred meters. It remains unclear whether this homing ability is restricted to the areas that had been previously explored or whether it allows the frogs to navigate from areas outside their direct experience. Here, we used radio-tracking to study the navigational performance of three-striped poison frog translocated outside the area of their routine movements (200-800 m). Translocated frogs returned to their home territory via a direct path from all distances and with little difference in orientation accuracy, suggesting a flexible map-like navigation mechanism. These findings challenge our current understanding of both the mechanisms and the sensory basis of amphibian orientation.
View details for PubMedID 29217629
Induced parental care in a poison frog: a tadpole cross-fostering experiment
JOURNAL OF EXPERIMENTAL BIOLOGY
2017; 220 (21): 3949–54
Understanding the external stimuli and natural contexts that elicit complex behaviours, such as parental care, is key in linking behavioural mechanisms to their real-life function. Poison frogs provide obligate parental care by shuttling their tadpoles from terrestrial clutches to aquatic nurseries, but little is known about the proximate mechanisms that control these behaviours. In this study, we used Allobates femoralis, a poison frog with predominantly male parental care, to investigate whether tadpole transport can be induced in both sexes by transferring unrelated tadpoles to the backs of adults in the field. Specifically, we asked whether the presence of tadpoles on an adult's back can override the decision-making rules preceding tadpole pick-up and induce the recall of spatial memory necessary for finding tadpole deposition sites. We used telemetry to facilitate accurate tracking of individual frogs and spatial analysis to compare movement trajectories. All tested individuals transported their foster-tadpoles to water pools outside their home area. Contrary to our expectation, we found no sex difference in the likelihood to transport or in the spatial accuracy of finding tadpole deposition sites. We reveal that a stereotypical cascade of parental behaviours that naturally involves sex-specific offspring recognition strategies and the use of spatial memory can be manipulated by experimental placement of unrelated tadpoles on adult frogs. As individuals remained inside their home area when only the jelly from tadpole-containing clutches was brushed on the back, we speculate that tactile rather than chemical stimuli trigger these parental behaviours.
View details for PubMedID 28864563
View details for PubMedCentralID PMC5702076
Relying on known or exploring for new Movement patterns and reproductive resource use in a tadpole-transporting frog
2017; 5: e3745
Animals relying on uncertain, ephemeral and patchy resources have to regularly update their information about profitable sites. For many tropical amphibians, widespread, scattered breeding pools constitute such fluctuating resources. Among tropical amphibians, poison frogs (Dendrobatidae) exhibit some of the most complex spatial and parental behaviors-including territoriality and tadpole transport from terrestrial clutches to ephemeral aquatic deposition sites. Recent studies have revealed that poison frogs rely on spatial memory to successfully navigate through their environment. This raises the question of when and how these frogs gain information about the area and suitable reproductive resources. To investigate the spatial patterns of pool use and to reveal potential explorative behavior, we used telemetry to follow males of the territorial dendrobatid frog Allobates femoralis during tadpole transport and subsequent homing. To elicit exploration, we reduced resource availability experimentally by simulating desiccated deposition sites. We found that tadpole transport is strongly directed towards known deposition sites and that frogs take similar direct paths when returning to their home territory. Frogs move faster during tadpole transport than when homing after the deposition, which probably reflects different risks and costs during these two movement phases. We found no evidence for exploration, neither during transport nor homing, and independent of the availability of deposition sites. We suggest that prospecting during tadpole transport is too risky for the transported offspring as well as for the transporting male. Relying on spatial memory of multiple previously discovered pools appears to be the predominant and successful strategy for the exploitation of reproductive resources in A. femoralis. Our study provides for the first time a detailed description of poison frog movement patterns during tadpole transport and corroborates recent findings on the significance of spatial memory in poison frogs. When these frogs explore and discover new reproductive resources remains unknown.
View details for PubMedID 28875083
Humans recognize emotional arousal in vocalizations across all classes of terrestrial vertebrates: evidence for acoustic universals
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
2017; 284 (1859)
Writing over a century ago, Darwin hypothesized that vocal expression of emotion dates back to our earliest terrestrial ancestors. If this hypothesis is true, we should expect to find cross-species acoustic universals in emotional vocalizations. Studies suggest that acoustic attributes of aroused vocalizations are shared across many mammalian species, and that humans can use these attributes to infer emotional content. But do these acoustic attributes extend to non-mammalian vertebrates? In this study, we asked human participants to judge the emotional content of vocalizations of nine vertebrate species representing three different biological classes-Amphibia, Reptilia (non-aves and aves) and Mammalia. We found that humans are able to identify higher levels of arousal in vocalizations across all species. This result was consistent across different language groups (English, German and Mandarin native speakers), suggesting that this ability is biologically rooted in humans. Our findings indicate that humans use multiple acoustic parameters to infer relative arousal in vocalizations for each species, but mainly rely on fundamental frequency and spectral centre of gravity to identify higher arousal vocalizations across species. These results suggest that fundamental mechanisms of vocal emotional expression are shared among vertebrates and could represent a homologous signalling system.
View details for PubMedID 28747478
View details for PubMedCentralID PMC5543225
Homing performance in a territorial dendrobatid frog, Allobates talamancae
2017; 53 (2): 309–13
View details for Web of Science ID 000401339600016
The significance of spatial memory for water finding in a tadpole-transporting frog
2016; 116: 89–98
The ability to associate environmental cues with valuable resources strongly increases the chances of finding them again, and thus memory often guides animal movement. For example, many temperate region amphibians show strong breeding site fidelity and will return to the same areas even after the ponds have been destroyed. In contrast, many tropical amphibians depend on exploitation of small, scattered and fluctuating resources such as ephemeral pools for reproduction. It remains unknown whether tropical amphibians rely on spatial memory for effective exploitation of their reproductive resources. Poison frogs (Dendrobatidae) routinely shuttle their tadpoles from terrestrial clutches to dispersed aquatic deposition sites. We investigated the role of spatial memory for relocating previously discovered deposition sites in an experimental population of the brilliant-thighed poison frog, Allobates femoralis, a species with predominantly male tadpole transport. We temporarily removed an array of artificial pools that served as the principal tadpole deposition resource for the population. In parallel, we set up an array of sham sites and sites containing conspecific tadpole odour cues. We then quantified the movement patterns and site preferences of tadpole-transporting males by intensive sampling of the area and tracking individual frogs. We found that tadpole-carrier movements were concentrated around the exact locations of removed pools and most individuals visited several removed pool sites. In addition, we found that tadpole-transporting frogs were attracted to novel sites that contained high concentrations of conspecific olfactory tadpole cues. Our results suggest that A. femoralis males rely heavily on spatial memory for efficient exploitation of multiple, widely dispersed deposition sites once they are discovered. Additionally, olfactory cues may facilitate the initial discovery of the new sites.
View details for PubMedID 28239185
View details for PubMedCentralID PMC5321284
Take the long way home: Behaviour of a neotropical frog, Allobates femoralis, in a detour task
2016; 126: 71–75
Detour behaviour, an individual's ability to reach its goal by taking an indirect route, has been used to test spatial cognitive abilities across a variety of taxa. Although many amphibians show a strong homing ability, there is currently little evidence of amphibian spatial cognitive flexibility. We tested whether a territorial frog, Allobates femoralis, can flexibly adjust its homing path when faced with an obstacle. We displaced male frogs from their calling sites into the centre of circular arenas and recorded their escape routes. In the first experiment we provided an arena with equally high walls. In the second experiment we doubled the height of the homeward facing wall. Finally, we provided a tube as a shortcut through the high wall. In the equal-height arena, most frogs chose to escape via the quadrant facing their former calling site. However, when challenged with different heights, nearly all frogs chose the low wall, directing their movements away from the calling site. In the "escape tunnel" experiment most frogs still chose the low wall. Our results show that displaced A. femoralis males can flexibly adjust their homing path and avoid (presumably energetically costly) obstacles, providing experimental evidence of spatial cognitive flexibility in an amphibian.
View details for PubMedID 26997105
View details for PubMedCentralID PMC5458138
Sex-specific offspring discrimination reflects respective risks and costs of misdirected care in a poison frog
2016; 114: 173–79
The ability to differentiate between one's own and foreign offspring ensures the exclusive allocation of costly parental care to only related progeny. The selective pressure to evolve offspring discrimination strategies is largely shaped by the likelihood and costs of offspring confusion. We hypothesize that males and females with different reproductive and spatial behaviours face different risks of confusing their own with others' offspring, and this should favour differential offspring discrimination strategies in the two sexes. In the brilliant-thighed poison frog, Allobates femoralis, males and females are highly polygamous, terrestrial clutches are laid in male territories and females abandon the clutch after oviposition. We investigated whether males and females differentiate between their own offspring and unrelated young, whether they use direct or indirect cues and whether the concurrent presence of their own clutch is essential to elicit parental behaviours. Males transported tadpoles regardless of location or parentage, but to a lesser extent in the absence of their own clutch. Females discriminated between clutches based on exact location and transported tadpoles only in the presence of their own clutch. This sex-specific selectivity of males and females during parental care reflects the differences in their respective costs of offspring confusion, resulting from differences in their spatial and reproductive behaviours.
View details for PubMedID 28239184
View details for PubMedCentralID PMC5321237
- High-resolution forest mapping for behavioural studies in the Nature Reserve 'Les Nouragues', French Guiana JOURNAL OF MAPS 2016; 12 (1): 26–32
Flexible compensation of uniparental care: female poison frogs take over when males disappear
2015; 26 (4): 1219–25
Parental care systems are shaped by costs and benefits to each sex of investing into current versus future progeny. Flexible compensatory parental care is mainly known in biparental species, particularly where parental desertion or reduction of care by 1 parent is common. The other parent can then compensate this loss by either switching parental roles and/or by increasing its own parental effort. In uniparental species, desertion of the caregiver usually leads to total brood loss. In the poison frog, Allobates femoralis, obligatory tadpole transport (TT) is generally performed by males, whereas females abandon their clutches after oviposition. Nevertheless, in a natural population we previously observed 7.8% of TT performed by females, which we could link to the absence of the respective fathers. In the following experiment, under laboratory conditions, all tested A. femoralis females flexibly took over parental duties, but only when their mates were removed. Our findings provide clear evidence for compensatory flexibility in a species with unisexual parental care. Contrary to the view of amphibian parental care as being stereotypical and fixed, these results demonstrate behavioral flexibility as an adaptive response to environmental and social uncertainty. Behavioral flexibility might actually represent a crucial step in the evolutionary transition from uniparental to biparental care in poison frogs. We suspect that across animal species flexible parental roles are much more common than previously thought and suggest the idea of a 3-dimensional continuum regarding flexibility, parental involvement, and timing, when thinking about the evolution of parental care.
View details for PubMedID 26167099
View details for PubMedCentralID PMC4495760
Poison frogs rely on experience to find the way home in the rainforest
2014; 10 (11): 20140642
Among vertebrates, comparable spatial learning abilities have been found in birds, mammals, turtles and fishes, but virtually nothing is known about such abilities in amphibians. Overall, amphibians are the most sedentary vertebrates, but poison frogs (Dendrobatidae) routinely shuttle tadpoles from terrestrial territories to dispersed aquatic deposition sites. We hypothesize that dendrobatid frogs rely on learning for flexible navigation. We tested the role of experience with the local cues for poison frog way-finding by (i) experimentally displacing territorial males of Allobates femoralis over several hundred metres, (ii) using a harmonic direction finder with miniature transponders to track these small frogs, and (iii) using a natural river barrier to separate the translocated frogs from any familiar landmarks. We found that homeward orientation was disrupted by the translocation to the unfamiliar area but frogs translocated over similar distances in their local area showed significant homeward orientation and returned to their territories via a direct path. We suggest that poison frogs rely on spatial learning for way-finding in their local area.
View details for PubMedID 25411379
View details for PubMedCentralID PMC4261859
Ravens notice dominance reversals among conspecifics within and outside their social group
2014; 5: 3679
A core feature of social intelligence is the understanding of third-party relations, which has been experimentally demonstrated in primates. Whether other social animals also have this capacity, and whether they can use this capacity flexibly to, for example, also assess the relations of neighbouring conspecifics, remains unknown. Here we show that ravens react differently to playbacks of dominance interactions that either confirm or violate the current rank hierarchy of members in their own social group and of ravens in a neighbouring group. Therefore, ravens understand third-party relations and may deduce those not only via physical interactions but also by observation.
View details for PubMedID 24755739
Homing trajectories and initial orientation in a Neotropical territorial frog, Allobates femoralis (Dendrobatidae)
FRONTIERS IN ZOOLOGY
2014; 11: 29
The ability to relocate home or breeding sites after experimental removal has been observed in several amphibians and the sensory basis of this behavior has been studied in some temperate-region species. However, the actual return trajectories have rarely been quantified in these studies and it remains unknown how different cues guide the homing behavior. Dendrobatidae (dart-poison frogs) exhibit some of the most complex spatial behaviors among amphibians, such as territoriality and tadpole transport. Recent data showed that Allobates femoralis, a frog with paternal tadpole transport, successfully returns to the home territories after experimental translocations of up to 400 m. In the present study, we used harmonic direction finding to obtain homing trajectories. Additionally, we quantified the initial orientation of individuals, translocated 10 m to 105 m, in an arena assay.Tracking experiments revealed that homing trajectories are characterized by long periods of immobility (up to several days) and short periods (several hours) of rapid movement, closely fitting a straight line towards the home territory. In the arena assay, the frogs showed significant homeward orientation for translocation distances of 35 m to 70 m but not for longer and shorter distances.Our results describe a very accurate homing behavior in male A. femoralis. The straightness of trajectories and initial homeward orientation suggest integration of learned landmarks providing a map position for translocated individuals. Future research should focus on the role of learning in homing behavior and the exact nature of cues being used.
View details for PubMedID 24666825
Tadpole transport logistics in a Neotropical poison frog: indications for strategic planning and adaptive plasticity in anuran parental care
FRONTIERS IN ZOOLOGY
2013; 10: 67
Individuals should aim to adjust their parental behaviours in order to maximize the success of their offspring but minimize associated costs. Plasticity in parental care is well documented from various bird, mammal and fish species, whereas amphibians were traditionally assumed as being highly instinct-bound. Therefore, little is known about 'higher' cognitive abilities of amphibians, such as strategic planning and behavioural flexibility. Dendrobatid frogs have evolved a remarkable diversity of parental behaviours. The most noticeable of these behaviours is tadpole transport, which is obligatory in almost all species. Nonetheless, there is limited knowledge about spatial and temporal patterns of tadpole transport and the possible existence of behavioural plasticity on the individual level. In this study, we investigated correlates of tadpole transport behaviour in a natural population of the dendrobatid frog Allobates femoralis during five years.Tadpole transport was predominantly observed during morning hours. Although tadpoles were carried almost exclusively by males (N = 119), we also observed ten females performing this task. The parentage analysis revealed that in all cases females transported their own offspring. In contrast, four tadpole-carrying males were not the genetic fathers of the larvae they were transporting. The average clutch size of 20 eggs and our observation of an average of 8 tadpoles on the back of transporting individuals indicate that frogs do not carry entire clutches at once, and/or that they distribute their larvae across several water bodies. Contrary to the predictions from a hypothetical random search for deposition sites, the number of transported tadpoles was higher in males that travelled over longer distances.Our results suggest a strong selective pressure on males to shift the time invested in tadpole transport to periods of low intra-specific competition. The number of tadpoles on the back of the males significantly correlated with displacement distance from the respective home territories, indicating a strategic non-random tadpole transport rather than random search for suitable tadpole deposition sites during tadpole transport. The observation of females who occasionally transported larvae supports the prevalence of adaptive plasticity in parental behaviours even in a species with a rather low level of parental care.
View details for PubMedID 24209580
The Homing Frog: High Homing Performance in a Territorial Dendrobatid Frog Allobates femoralis (Dendrobatidae)
2013; 119 (9): 762–68
Dendrobatidae (dart-poison frogs) exhibit some of the most complex spatial behaviors among amphibians, such as territoriality and tadpole transport from terrestrial clutches to widely distributed deposition sites. In species that exhibit long-term territoriality, high homing performance after tadpole transport can be assumed, but experimental evidence is lacking, and the underlying orientation mechanisms are unknown. We conducted a field translocation experiment to test whether male Allobates femoralis, a dendrobatid frog with paternal extra-territorial tadpole transport, are capable of homing after experimental removal, as well as to quantify homing success and speed. Translocated individuals showed a very high homing success for distances up to 200 m and successfully returned from up to 400 m. We discuss the potential orientation mechanisms involved and selective forces that could have shaped this strong homing ability.
View details for PubMedID 25104869
Characterization of seven new polymorphic microsatellite loci in the brilliant-thighed poison frog Allobates femoralis (Dendrobatidae), and their cross-species utility in three other dendrobatid species
2013; 23 (3): 175–78
Here we document the development of seven novel polymorphic microsatellite markers for the brilliant-thighed poison frog Allobates femoralis (Dendrobatidae). We found between six and 27 alleles per locus in 100 individuals (50 males, 50 females) from the field site 'Saut Pararé', French Guiana, with an average observed heterozygosity of 0.79. One locus (Afem23) deviated significantly from Hardy-Weinberg equilibrium. We did not find any evidence for linkage disequilibrium among the new loci, or to seven of the already described markers for A. femoralis. We also report cross-species amplification of some of the markers in three other dendrobatid species (A. talamancae, Dendrobates tinctorius and Oophaga pumilio).
View details for PubMedID 25110383
View details for PubMedCentralID PMC4126724