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Social animals need to keep track of other individuals in their group to be able to adjust their behaviour accordingly and facilitate group cohesion. This recognition ability varies across species and is influenced by cognitive capacities such as learning and memory. In reptiles, particularly Squamates (lizards, snakes, and worm lizards), chemical communication is pivotal for territoriality, reproduction, and other social interactions. However, the cognitive processes underlying these social interactions remain understudied. In our study, we examined the ability of male and female Tokay geckos (Gekko gecko) to chemically differentiate familiar and unfamiliar mating partners. Our findings suggest that both sexes can make this distinction, with males responding more to the odour of a familiar mate, and females responding more to unfamiliar mates. The lizards maintained their discriminatory abilities for two to three weeks but not up to six weeks after separation. This research highlights the efficacy of using odours as social stimuli for investigating social cognition in lizards, a promising avenue to better understand social cognition in these animals.
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Lagartos , Reconocimiento en Psicología , Animales , Lagartos/fisiología , Femenino , Masculino , Conducta Sexual Animal , Odorantes , Discriminación en PsicologíaRESUMEN
Animals constantly need to evaluate available external and internal information to make appropriate decisions. Identifying, assessing, and acting on relevant cues in contexts such as mate choice, intra-sexual competition, and parental care is particularly important for optimizing individual reproductive success. Several factors can influence decision-making, such as external environmental cues and the animal's own internal state, yet, we have limited knowledge on how animals integrate available information. Here, we used an entire island population (57 males, 53 females, and 1,109 tadpoles) of the neotropical brilliant-thighed poison frog Allobates femoralis to investigate how 2 factors (olfactory cues and personality traits) influence the ability of males to find and use new resources for tadpole deposition. We experimentally manipulated the location of tadpole deposition sites and their associated olfactory cues, and repeatedly measured exploration and boldness in adult males. We further reconstructed tadpole deposition choices via inferred parent-offspring relationships of adult frogs and tadpoles deposited in our experimental pools using molecular parentage analysis. We found that the discovery and use of new rearing sites were heavily influenced by olfactory cues; however, we did not find an effect of the measured behavioral traits on resource discovery and use. We conclude that in highly dynamic environments such as tropical rainforests, reliable external cues likely take priority over personality traits, helping individuals to discover and make use of reproductive resources.
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Animals constantly need to evaluate available external and internal information to make appropriate decisions. Identifying, assessing, and acting on relevant cues in contexts such as mate choice, intra-sexual competition, and parental care is particularly important for optimizing individual reproductive success. Several factors can influence decision-making, such as external environmental cues and the animal's own internal state, yet, we have limited knowledge on how animals integrate available information. Here, we used an entire island population (57 males, 53 females, and 1,109 tadpoles) of the neotropical brilliant-thighed poison frog Allobates femoralis to investigate how 2 factors (olfactory cues and personality traits) influence the ability of males to find and use new resources for tadpole deposition. We experimentally manipulated the location of tadpole deposition sites and their associated olfactory cues, and repeatedly measured exploration and boldness in adult males. We further reconstructed tadpole deposition choices via inferred parent-offspring relationships of adult frogs and tadpoles deposited in our experimental pools using molecular parentage analysis. We found that the discovery and use of new rearing sites were heavily influenced by olfactory cues; however, we did not find an effect of the measured behavioral traits on resource discovery and use. We conclude that in highly dynamic environments such as tropical rainforests, reliable external cues likely take priority over personality traits, helping individuals to discover and make use of reproductive resources.
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In males, large testes size signifies high sperm production and is commonly linked to heightened sperm competition levels. It may also evolve as a response to an elevated risk of sperm depletion due to multiple mating or large clutch sizes. Conversely, weapons, mate or clutch guarding may allow individuals to monopolize mating events and preclude sperm competition, thereby reducing the selection of large testes. Herein, we examined how paternal care, sexual size dimorphism (SSD), weaponry and female fecundity are linked to testes size in glassfrogs. We found that paternal care was associated with a reduction in relative testes size, suggesting an evolutionary trade-off between testes size and parenting. Although females were slightly larger than males and species with paternal care tended to have larger clutches, there was no significant relationship between SSD, clutch size and relative testes size. These findings suggest that the evolution of testes size in glassfrogs is influenced by sperm competition risk, rather than sperm depletion risk. We infer that clutch guarding precludes the risk of fertilization by other males and consequently diminishes selective pressure for larger testes. Our study highlights the prominent role of paternal care in the evolution of testes size in species with external fertilization.
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Responsabilidad Parental , Testículo , Humanos , Masculino , Femenino , Animales , Semen , Espermatozoides/fisiología , Reproducción , Conducta Sexual Animal/fisiologíaRESUMEN
Hormones play a fundamental role in mediating social behaviors of animals. However, it is less well understood to what extent behavioral variation between individuals can be attributed to variation in underlying hormonal profiles. The goal of the present study was to infer if individual androgen levels, and/or the modulation thereof, can explain among-individual variation in aggressiveness, boldness and exploration. We used as a model the dart-poison frog Allobates femoralis and took repeated non-invasive water-borne hormonal samples of individual males before (baseline) and after (experimental) a series of behavioral tests for assessing aggression, boldness, and exploratory tendency. Our results show that androgen levels in A. femoralis are quite stable across the reproductive season. Repeatability in wbT baseline levels was high, while time of day, age of the frog, and trial order did not show any significant impact on measured wbT levels. In general, experimental wbT levels after behavioral tests were lower compared to the respective baseline levels. However, we identified two different patterns with regard to androgen modulation in response to behavioral testing: individuals with low baseline wbT tended to have increased wbT levels after the behavioral testing, while individuals with comparatively high baseline wbT levels rather showed a decrease in hormonal levels after testing. Our results also suggest that baseline wbT levels are linked to the personality trait exploration, and that androgen modulation is linked to boldness in A. femoralis males. These results show that differences in hormonal profiles and/or hormonal modulation in response to social challenges can indeed explain among-individual differences in behavioral traits.
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Andrógenos , Ranas Venenosas , Humanos , Animales , Masculino , Testosterona , Conducta Social , AguaRESUMEN
One of the most extreme adaptations to terrestriality in anurans is direct development, where eggs from terrestrial clutches entirely circumvent an aquatic tadpole stage and directly develop into small froglets. We here report the first case of egg-burying behaviour in a neotropical direct-developing frog with subsequent short-term maternal care. An amplectant pair of Pristimantis chocoensis was found at the Reserva Canandé in Esmeraldas, Ecuador, and we recorded oviposition and the later rotation and active burying of the clutch by the female. Both parents remained close to the nest area the following day. This rare observation sheds light on the complex but often cryptic reproductive behaviours of terrestrial amphibians and suggests that the evolution of direct development has selected for highly specialized forms of parental care.
Una de las adaptaciones más extremas a la terrestreidad en los anuros es el desarrollo directo, donde los huevos de puestas terrestres evitan por completo la etapa de renacuajo acuático y se desarrollan directamente en versiones miniatura de los adultos. Aquí informamos el primer caso de comportamiento de enterrar huevos en una rana neotropical de desarrollo directo con posterior cuidado materno a corto plazo. Una pareja amplectante de Pristimantis chocoensis fue encontrada en la Reserva Canandé en EsmeraldasEcuador, y registramos la oviposición y la posterior rotación y enterramiento activo de la puesta por parte de la hembra. Ambos padres permanecieron cerca del área del nido durante el día siguiente. Esta rara observación arroja luz sobre los complejos, pero a menudo crípticos, comportamientos reproductivos de los anfibios terrestres y sugiere que la evolución del desarrollo directo ha seleccionado formas altamente especializadas de cuidado parental.
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Individual reproductive success has several components, including the acquisition of mating partners, offspring production, and offspring survival until adulthood. While the effects of certain personality traits-such as boldness or aggressiveness-on single components of reproductive success are well studied, we know little about the composite and multifaceted effects behavioural traits can have on all the aspects of reproductive success. Behavioural traits positively linked to one component of reproductive success might not be beneficial for other components, and these effects may differ between sexes. We investigated the influence of boldness, aggressiveness, and exploration on the number of mating partners, mating events, and offspring surviving until adulthood in males and females of the Neotropical poison frog Allobates femoralis. Behavioural traits had different-even opposite-effects on distinct components of reproductive success in both males and females. For example, males who displayed high levels of aggressiveness and exploration (or low levels of aggressiveness and exploration) managed to attract high number of mating partners, while males with low levels of boldness, low levels of aggressiveness, and high levels of exploration had the most offspring surviving until adulthood. Our results therefore suggest correlational selection favouring particular combinations of behavioural traits.
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Agresión , Reproducción , Femenino , Masculino , Animales , Anuros , Comunicación Celular , PersonalidadRESUMEN
Animal personality traits are sometimes linked to an individual's degree of plasticity, with certain personality types being more plastic than others. In territorial species, consistently high levels of aggression might increase the risk of harmful fights, while consistently low aggression might lead to the loss of a territory. Consequently, reacting plastically with an appropriate territorial response should be beneficial to avoid these risks. An integrative investigation of both personality traits and plasticity can help us better understand the dynamics of aggressive interactions during male-male competition. Here, we used a free-ranging Neotropical poison frog population to investigate the role of plasticity in male territorial aggression towards intruders. We conducted repeated standardized territorial intrusion experiments mimicking frogs of different body sizes via playback calls with different peak frequencies. We found individual repeatability for the latency to reach and approach a simulated intruder and observed that both aggressive and less aggressive males decreased their level of aggression towards big intruders. However, our results do not support a correlation between personality and plasticity in the context of male territory defense during the breeding season. We discuss how such a correlation between personality and plasticity might be conditional on the costs and benefits across contexts.
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Trastornos de la Personalidad , Personalidad , Masculino , Animales , Anuros , Agresión , Tamaño CorporalRESUMEN
The most serious complication in the treatment of hemophilia A (HA) is the development of factor (F)VIII inhibitors or antidrug antibodies (ADA) occurring in 25-35% of patients with severe HA. The immunological mechanisms underlying the development of ADA against FVIII products have not been completely understood yet. Immunological danger signals associated with events such as infection or surgery have been suggested to play a critical role. In previous studies, we demonstrated that plasma-derived (pd)FVIII but not recombinant (r)FVIII can activate human monocyte-derived dendritic cells (DC) in a danger signal-dependent manner, which subsequently mediate the proliferation of autologous CD4+ T cells. In this study, we investigated the ability of plasma components, naturally present in pdFVIII products, to mediate T-cell responses. In fact, we show that addition of plasma to rFVIII plus lipopolysaccharide (LPS)-stimulated DC induces proliferation of autologous CD4+ T cells. Interestingly, although DC pulsed with LPS plus plasma induce T-cell proliferation upon co-culture, the addition of FVIII significantly increases the number of proliferating as well as FVIII-specific CD4+ T cells. Total proliferating CD4+ T cells and FVIII-specific subsets were identified mainly as central memory T cells. Experiments using blocking antibodies and receptor antagonists revealed that the complement proteins C3a and, to a lesser extent, C5a are critically involved in these LPS-mediated T-cell responses. Collectively, our results indicate that complement proteins are potent drivers of T-cell responses to FVIII. Data presented provide a model how event-related substitution of FVIII in HA patients might contribute to inhibitor development.
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Hemofilia A , Lipopolisacáridos , Humanos , Lipopolisacáridos/farmacología , Factor VIII , Hemofilia A/tratamiento farmacológico , Linfocitos T CD4-Positivos , Activación de Linfocitos , AnticuerposRESUMEN
Self-recognition is the ability to recognise stimuli originating from oneself. Humans and some non-human animals show evidence of true visual self-recognition in the mirror test. They use their reflection to inspect themselves and to remove a mark that is only visible in the mirror. Not all animals, however, rely primarily on vision. In lizards, chemical cues are crucial in social interactions, and therefore, lizards would benefit from a chemical self-other distinction. Here, we test the tokay gecko (Gekko gecko), a social species, on their ability to discriminate their own skin and faecal chemicals from those of same-sex, unfamiliar conspecifics. We predicted that individuals would show more self-directed behaviour when confronted with the chemicals from unfamiliar individuals within their home enclosure as a sign of the need for increased comparison. Geckos showed higher self-directed responses towards chemicals from unfamiliar individuals compared to self-produced chemicals and a water control. Furthermore, scat and skin chemicals (regardless of origin) elicited similar but stronger responses than peppermint oil pointing towards a possible social function of scat piles. Although further tests and controls are needed, our study provides evidence towards chemical self-recognition and for a social function of scat piling in tokay geckos.
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Lagartos , Humanos , Animales , Señales (Psicología) , HecesRESUMEN
Neophobia, the fear of novelty, is an ecologically important response which enables animals to avoid potentially harmful situations. Neophobia is a cognitive process by which individuals distinguish novelty from familiarity. In this study, we aimed to quantify this cognitive process in captive tokay geckos (Gekko gecko) across three contexts: when encountering novel prey, foraging near novel objects and entering a novel space. We also investigated individual consistency across trials using different novel stimuli, and correlation of individual responses across the three contexts. We found that geckos hesitate to attack novel prey and prey close to objects (familiar and novel). Geckos hesitated the most when entering novel space. Repeatability of behaviour within and across contexts was low (R = 0.101-0.190) indicating that neophobia might not be expressed similarly across contexts. The strength of a neophobic response can indicate how anxious or curious an individual is. This test has great potential to help answer questions about how captivity, enrichment, rearing environment and cognition affect fear responses in different contexts in lizards. By studying reptiles, we can better understand the universality of what is known about the causes leading to difference in neophobia across individuals and species.
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Lagartos , Animales , Miedo , Conducta ExploratoriaRESUMEN
The optimal foraging theory posits that animals aim to maximize energy intake while minimizing predation and handling costs during foraging. Most observed animal behaviour supports this theory, but occasional deviations provide insights into the ecological factors that shape foraging decisions. We tested prey-size preference using a two-choice test between different prey sizes in tokay geckos. We expected geckos to prefer larger prey and decision latencies to be longer when discrimination was more difficult and when small prey was offered. Geckos preferred larger prey when the size difference was large, although decision latency remained consistent. This aligns with prior research on sit-and-wait predators. Together with previous findings showing freezing behaviour after prey capture in tokay geckos, our findings suggest a strong influence of predator avoidance on foraging decisions opening up a new avenue for future research investigating the link between decision making and predator avoidance in tokay geckos.
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Environmental variation plays a key role in the evolution and maintenance of animal personality. Individuals with different personality types might exhibit different habitat preferences. Alternatively, variation in individual behaviour across space could arise as a plastic adaptation to distinct habitats. Our study aims to investigate if habitat choice is influenced by an individual's personality. We assessed individual levels of activity, boldness, and exploration in male poison frogs, and performed a habitat choice test under controlled laboratory conditions. Individuals were consistent in their behaviours, but all tested frogs chose the complex over the simple habitat. Individuals that were characterized as bold and very explorative also showed more movements between the two different habitats in the choice test. These results indicate that personality measured in a highly standardized artificial setup, such as a novel environment test, indeed can reflect boldness and exploration related behaviours measured in a more naturalistic setup.
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Animals often show consistency in their behavioural repertoire across time and/or contexts that differs from other individuals of the same population, i.e. animal personality. We currently have quite an incomplete understanding of the factors that lead to behavioural traits remaining stable - or becoming decoupled - over an animal's lifetime. In this study, we investigated the role of metamorphosis in the development of animal personality in a Neotropical poison frog, a species that undergoes drastic morphological and ecological changes during its development. We used lab-reared individuals of the brilliant-thighed poison frog Allobates femoralis to assess if consistent individual differences are already present at the tadpole stage, and if these differences are maintained throughout metamorphosis. We found evidence for two personality traits, exploration and boldness, already present in A. femoralis tadpoles. Despite the drastic changes in morphology, physiology, and habitat in the transition from tadpoles to metamorphs, personality traits persisted throughout metamorphosis, suggesting a physiological and/or genetic basis for the measured behavioural traits. We also found that exploration and boldness related behaviours were correlated with growth speed. Very bold and explorative individuals took fewer days until metamorphosis compared to very shy and non-explorative ones, which is in line with the concept of a Pace-of-Life Syndrome. These findings provide important insights into the proximate mechanisms that generate personality in species with complex life cycles.
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Parenting is considered a key evolutionary innovation that contributed to the diversification and expansion of vertebrates. However, we know little about how such diversity evolved. Amphibians are an ideal group in which to identify the ecological factors that have facilitated or constrained the evolution of different forms of parental care. Among, but also within, the three amphibian orders-Anura, Caudata, and Gymnophiona-there is a high level of variation in habitat use, fertilization mode, mating systems, and parental sex roles. Recent work using broad phylogenetic, experimental, and physiological approaches has helped to uncover the factors that have selected for the evolution of care and transitions between different forms of parenting. Here, we highlight the exceptional diversity of amphibian parental care, emphasize the unique opportunities this group offers for addressing key questions about the evolution of parenting, and give insights into promising novel directions of research.
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Sex differences in vertebrate spatial abilities are typically interpreted under the adaptive specialization hypothesis, which posits that male reproductive success is linked to larger home ranges and better navigational skills. The androgen spillover hypothesis counters that enhanced male spatial performance may be a byproduct of higher androgen levels. Animal groups that include species where females are expected to outperform males based on life-history traits are key for disentangling these hypotheses. We investigated the association between sex differences in reproductive strategies, spatial behavior, and androgen levels in three species of poison frogs. We tracked individuals in natural environments to show that contrasting parental sex roles shape sex differences in space use, where the sex performing parental duties shows wider-ranging movements. We then translocated frogs from their home areas to test their navigational performance and found that the caring sex outperformed the non-caring sex only in one out of three species. In addition, males across species displayed more explorative behavior than females and androgen levels correlated with explorative behavior and homing accuracy. Overall, we reveal that poison frog reproductive strategies shape movement patterns but not necessarily navigational performance. Together this work suggests that prevailing adaptive hypotheses provide an incomplete explanation of sex differences in spatial abilities.
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Anuros , Conducta Animal , Animales , Femenino , Masculino , Andrógenos , Anuros/fisiología , Factores Sexuales , Conducta Animal/fisiologíaRESUMEN
To make decisions, animals gather information from the environment in order to avoid costs (e.g., reduced survival) and increase benefits (e.g., foraging success). When time is limited or information is insufficient, most animals face a speed-accuracy trade-off (SAT) - they have to balance the benefits of making quick decisions against the costs of inaccurate decisions. Here, we investigated the relationship between decision accuracy and decision speed in gidgee skinks (Egernia stokesii) performing a food-based spontaneous quantity discrimination task. Rather than a SAT we found a speed-accuracy alignment; lizards made decisions that were fast and accurate, rather than inaccurate. Furthermore, we found only within-, but no between-individual differences in decision making indicating behavioural plasticity in the absence of individual decision styles. Finally, latency to choice was highly repeatable, more so than choice accuracy. Previous work has shown that learning, the costs of a bad decision and task difficulty frequently result in SATs. The lack of a SAT in our lizards might be a direct consequence of our simple testing methodology which prevented learning by not allowing lizards to consume the chosen quantity. To fully understand how SATs develop, different methodologies that control the costs and benefits of decisions should be compared.
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Lagartos , Animales , Toma de Decisiones , RecompensaRESUMEN
Territoriality has been widely described across many animal taxa, where the acquisition and defence of a territory are critical for the fitness of an individual. Extensive evidence suggests that androgens are involved in the modulation of territorial behaviours in male vertebrates. Short-term increase of androgen following a territorial encounter appears to favour the outcome of a challenge. The "Challenge Hypothesis" proposed by Wingfield and colleagues outlines the existence of a positive feedback relationship between androgen and social challenges (e.g., territorial intrusions) in male vertebrates. Here we tested the challenge hypothesis in the highly territorial poison frog, Allobates femoralis, in its natural habitat by exposing males to simulated territorial intrusions in the form of acoustic playbacks. We quantified repeatedly androgen concentrations of individual males via a non-invasive water-borne sampling approach. Our results show that A. femoralis males exhibited a positive behavioural and androgenic response after being confronted to simulated territorial intrusions, providing support for the Challenge Hypothesis in a territorial frog.
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Andrógenos , Territorialidad , Agresión/fisiología , Andrógenos/farmacología , Andrógenos/fisiología , Animales , Anuros , Conducta Animal/fisiología , Masculino , TestosteronaRESUMEN
Background: The Tropical Andes is the world's most biodiverse hotspot. This region contains >1,000 amphibian species, more than half of which are endemic. Herein we describe two new glassfrog species (Centrolenidae: Hyalinobatrachium) that we discovered within relatively unexplored and isolated localities of the Ecuadorian Andes. Methods: We employed morphological, acoustic, and molecular methods to test the hypothesis that Hyalinobatrachium mashpi sp. nov and H. nouns sp. nov. are species new to science. Following standard methods, we generated mitochondrial sequences (16S) of 37 individuals in the genus Hyalinobatrachium. We inferred the phylogenetic relationships of the two new species in comparison to all other glassfrogs using Maximum Likelihood. In addition to describing the call of H. mashpi sp. nov., we performed a discriminant analysis of principal components (DAPC) with the advertisement call characteristics of several congeners. Results: Based on an integrative taxonomy approach, we describe two new species. Morphological traits and the inferred phylogeny unambiguously place the new taxa in the genus Hyalinobatrachium. Both species are distinguished from other glassfrogs mainly by their dorsal coloration (i.e., dorsum lime green with small light yellow spots, head usually with interorbital bar) and transparent pericardium (i.e., the heart is visible through the ventral skin). The new species exhibit a high morphological similarity (i.e., cryptic) and occur within relatively close geographical proximity (closest aerial distance = 18.9 km); however, their uncorrected p distance for the mitochondrial gene 16S is 4.6-4.7%, a value that greatly exceeds the genetic distance between closely related species of centrolenid frogs. The DAPC revealed that the advertisement call of H. mashpi sp. nov. is acoustically distinct. Discussion: Our findings are congruent with several previous studies that report a high degree of endemism in the Toisán mountain range, which appears to be isolated from the main Andean cordillera for some amphibian groups. We recommend that both H. mashpi sp. nov. and H. nouns sp. nov. be listed as Endangered, following IUCN criteria. These new species provide another example of cryptic diversity in the Andes-further evidence that the region fosters much more biodiversity than we have the resources to catalog. Threatened by mining and other exploitative industries, these glassfrogs and many other yet-to-be-discovered Andean species highlight the dire need for effective conservation measures-especially in northwestern Ecuador.
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Anuros , Biodiversidad , Animales , Anuros/genética , Ecuador , Genes Mitocondriales , FilogeniaRESUMEN
In many animal species, members of one sex, most often females, exhibit a strong preference for mating partners with particular traits or resources. However, when females sequentially mate with multiple partners, strategies underlying female choice are not very well understood. Particularly, little is known if under such sequential polyandry females mate truly randomly, or if they actively try to spread mating events across multiple partners. In the present study, we used the highly promiscuous poison frog Allobates femoralis to investigate whether promiscuity could result from a preference for novel mates. Furthermore, we examined the importance of call characteristics for mate choice. We conducted mate choice experiments in a laboratory setup, by presenting females with recent mating partners or novel males. We recorded call characteristics of both males and the time females spent close to each male. In our trials, females preferred previous mating partners over novel males and also males with shorter advertisement calls. Results from previous studies on A. femoralis suggest that females in our trials recognized previous partners based on individual call characteristics. While mating decisions in the wild and in the laboratory might differ, our study provides first evidence for female mate choice in a poison frog with sequential polyandry.