Max Ringler currently works at the Department of Ecology and Evolutionary Biology, University of California, Los Angeles. Max does research in behavioural ecology, tropical ecology, and herpetology with a special focus on bioacoustics and GIS methods. Their current projects are 'Social structures in amphibians – communication networks (CN) and social networks (SN) in the Neotropical frog Allobates femoralis.' and 'Movement ecology and spatial cognition of tropical amphibians'.
Skills and Expertise
Research Items (75)
Social complexity arises from the formation of social relationships like social bonds and dominance hierarchies. In turn, these aspects may be affected by the degree of fission-fusion dynamics, i.e., changes in group size and composition over time. Whilst fission-fusion dynamics has been studied in mammals, birds have received comparably little attention, despite some species having equally complex social lives. Here, we investigated the influence of environmental factors on aspects of fission-fusion dynamics in a free-ranging population of carrion and hooded crows (Corvus corone ssp.) in the urban zoo of Vienna, Austria over a 1-year period. We investigated 1) the size and 2) spatio-temporal structure of the local flock, and 3) environmental influences on local flock and subgroup size. The local flock size varied considerably over the year, with fewest birds being present during the breeding season. The spatio-temporal structure of the local flock showed 4 distinct presence categories, of which the proportions changed significantly throughout the year. Environmental effects on both local flock and subgroup size were time of day, season, temperature, and weather, with additional pronounced effects of the structure of the surroundings and age class on subgroup size. Our findings show environmental influences on party size at the local flock and subgroup level, as well as indications of structured party composition in respect to the 4 presence categories. These results suggest that environmental factors have significant effects on fission-fusion dynamics in free-ranging crows, thereby influencing social complexity.
Question - Individual identification SNP software?
Some territorial animals recognize familiar neighbours and are less aggressive to established neighbours than they are to strangers. This form of social recognition produces a ‘dear enemy’ effect, which may allow animals to reduce the costs of territory defence. The dear enemy effect is thought to reflect either the decreased threat posed by neighbours relative to strangers (the relative threat hypothesis) or the decreased need for escalation with increasing familiarity between neighbours (the familiarity hypothesis). We tested for a vocally mediated dear enemy effect in male brilliant-thighed poison frogs, Allobates femoralis. In this species, the familiarity hypothesis predicts a dear enemy effect, because males defend long-term stable territories and should be familiar with the calls of their neighbours. In contrast, the relative threat hypothesis does not predict a dear enemy effect, because neighbours and strangers both represent competitors for mates and likely pose equivalent threats. Acoustic analyses showed that males produce individually distinctive advertisement calls. Two playback experiments were conducted to determine whether territorial males respond less aggressively to neighbours' calls than to strangers' calls based on this acoustic identity information. In the first experiment, males pursued acoustically simulated neighbours and strangers to similar distances when calls were played both from the direction of the neighbour's territory and from a direction with no neighbours. In the second experiment, males responded aggressively to neighbours' and strangers' calls at similar threshold amplitudes and pursued these calls to similar distances. Hence, two different playback experiments failed to find evidence of a vocally mediated dear enemy effect. Our results support the hypothesis that territorial animals respond to the relative threat posed by neighbours and strangers regardless of their level of familiarity with neighbours.
Question - Infrared thermometer for very small frogs?
With Amphibians and IR measurements/imagery one thing you also need to consider is that moist skin, like with photo cameras will give you all sorts of reflections, also in the IR part of the spectrum, and especially under varying, natural illumination conditions. So to make meaningful measurements of (small) frog surfaces, unless it is a mostly dry skinned species, you will have to somehow overshadow the frog to make sure it is actual IR emission,and not IR reflections from the sun that you are measuring. Of course this then comes with severe constraints in terms of not disturbing frogs and is also the reason why we mostly switched to measure substrate surface temperatures of perches immediately after the frog moved away. But of course I understand there are circumstances where the actual surface temperature of the frog can be of interest!
Question - Infrared thermometer for very small frogs?
as these devices use (infread) light through special optics, the problem is mainly a physical one. Think of you request as the analogue to a telephoto-lens which should give you maximum magnification (small spot size) over maximum distance (minimal disturbance). With photo cameras, such lenses get huge and very expensive pretty quick, and such is the case with IR thermometers. Now FLIR cameras do nothing but replacing the single temperature sensor with a 2-dimensional image chip that can detect IR, analogous to the chip in a photo camera. Then detection area theoretically is limited by the pixel size, however, as each pixel is considerably smaller as the sensor of a IR meter, also accuracy will be reduced, as less photons will be received per sensor site/pixel, and you will end up with noise the smaller the pixels (sensor).
What is the exact purpose of your measurements? As you emphasize minimal disturbance I assume you want to measure body temperature of frogs that are resting or calling on a substrate for a while already (not moving, and you don't want to scare them away). As poikolotherms, the frogs will, by and large, have the same temperature as their substrate unless two things are the case - 1. either they are capable to produce some heat internally, or 2. they have (considerably large) different heat absorbance characteristics than the substrate they are sitting on, causing them to heat up either more or less then then substrate.
To detect this latter case of frogs having a body temperature which deviates considerably from their substrate temperature, you still can make differential measurements, (mostly) regardless of the spot size of your IR meter - so male one measurement with the frog covering as much as possible of the spot, and one of the substrate directly beside the frog. However, as I said the effect you want to measure has to be quite strong, as also the accuracy of IR thermometers in the price range you specified is mostly within 0.5-1 °C (although they give readings at0.1 °C).
So long story short, unless the purpose of your study is to measure (tiny) temperature difference across (within) the surface of a frog, and with the money you state you have available, you will be fine with IR thermometers with a spot size within 1-3 times the SUL of the frogs you want to measure.These devices mostly have optics with a distance to spot ratio of 20:1 - so at 20 cm distance your spot size is 1 cm in diameter, at 40 cm its 2, ... at 1 m its 5 cm and so on. Also they often are available at different calibration qualities (accuracies) which problaby should be of equal, if not even more concern as the spot size.
Hope these ideas help a little
Parental decisions in animals are often context‐dependent and shaped by fitness trade‐offs between parents and offspring. For example, the selection of breeding habitats can considerably impact the fitness of both offspring and parents, and therefore parents should carefully weigh the costs and benefits of available options for their current and future reproductive success. Here we show that resource‐use preferences are shaped by a trade‐off between parental effort and offspring safety in a tadpole‐transporting frog. In a large‐scale in‐situ experiment, we investigated decision‐strategies across an entire population of poison frogs that distribute their tadpoles across multiple water bodies. Pool use followed a dynamic and sequential selection process and transportation became more efficient over time. Our results point to a complex suite of environmental variables that are considered during offspring deposition, which necessitates a highly dynamic and flexible decision‐making process in tadpole‐transporting frogs. This article is protected by copyright. All rights reserved.
Question - Circular statistics - ecology - softwares, methods and recommendations?
Oriana (https://www.kovcomp.co.uk/oriana/), a stat program specialised on circular statistics, has a 30-day free trial. PAST (https://folk.uio.no/ohammer/past/) has some circular stats functionality. And in R you have the 'circular' package: https://cran.r-project.org/web/packages/circular/
P.S.: Check you g-mailbox ;-)
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.
Tagged male tadpole carrier The tag consists of a silicon tube around the waist, with an additional silicone strap between the hind legs, a small diode (beneath the white sealing) and a dipole antenna made of flexible coated wire.
Movement precision during tadpole transport Summarized data of the average angular deviation, average distance from the straight-line path and SC for the tadpole transport of frogs which encountered only available pools during tadpole transport (A) and frogs which encountered non-available pools (N), minimum, maximum, 1st and 3rd quartile, median and mean.
Movement precision during homing Summarized data of the average angular deviation, average distance from the straight-line path and SC for the homing trajectories of frogs which encountered only available pools during tadpole transport (A) and frogs which encountered non-available pools (N), minimum, maximum, 1st and 3rd quartile, median and mean.
Homing trajectories Trajectory map showing movement patterns of frogs homing back to their territory after tadpole transport. Red asterisks represent the territory centers of tracked carriers and colored lines show different tracking events. Squares represent the cross-array of thirteen artificial tadpole deposition sites, blue squares representing available pools and gray crossed squares the removed deposition sites. Blue circles represent four potential natural pools, which were visited by tadpole carriers during tracking. Contour lines (1 m) and the Arataye River are drawn in light gray.
Summarized results of homing trajectories Each row represents a specific tracking event. Columns show the tracked distance during homing, straight line distance (from the last deposition site to the territory center), duration of homing, whether homing took more than one day (overnight = 1), average speed and the straightness coefficient.
Summarized results of tadpole transport trajectories Each row represents a specific tracking event. Columns show the frog ID, number of tadpoles, tracked distance, total time of the tracked path (h), average speed (m/h) across the entire TTs, number of deposition sites visited (in parentheses the number of available (a) and non-available (n) deposition sites), total estimated tadpole transport distance, straight-line distance (from the territory centroid across all deposition site until all tadpoles were deposited) and a straightness coefficient.
Acoustic ranging allows identifying the distance of a sound source and mediates inter-individual spacing and aggression in territorial species. Birds and mammals are known to use more complex cues than only sound pressure level (SPL), which can be influenced by the signaller and signal transmission in non-predictable ways and thus is not reliable by itself. For frogs, only SPL is currently known to mediate inter-individual distances, but we hypothesise that the strong territoriality of Dendrobatids could make the use of complex cues for ranging highly beneficial for this family. Therefore, we tested the ranging abilities of territorial males of Allobates femoralis (Dendrobatidae, Aromobatinae) in playback trials, using amplitude-normalized signals that were naturally degraded over distance, and synthetic signals that were masked with different levels of noise. Frogs responded significantly less to signals recorded from larger distances, regardless of SPL and signal-to-noise ratio (SNR), but showed no differential response to natural minimum and maximum SNRs across the typical communication range in wild populations. This indicates that frogs used signal amplitude and SNR only as ancillary cues when assessing the distance of sound sources and relied instead mainly on more complex cues, such as spectral degradation or reverberation. We suggest that this ability mediates territorial spacing and mate choice in A. femoralis. Good ranging abilities might also play a role in the remarkable orientation performance of this species, probably by enabling the establishment of a mental acoustic map of the habitat. Significance statement Acoustic ranging allows the distance of vocalizing competitors and mates to be identified. While birds and mammals are known to use complex cues such as temporal degradation, frequency-dependent attenuation and reverberation for ranging, previous research indicated that frogs rely only on signal amplitude (sound pressure level) to assess the distance of other callers. The present study shows for the first time that also poison frogs can make use of more complex cues, an ability which is likely to be highly beneficial in their territorial social organization and probably can also be used for orientation. Electronic supplementary material The online version of this article (doi:10.1007/s00265-017-2340-2) contains supplementary material, which is available to authorized users.
Question - Does anyone know of microsatellite discovery and primer design services in Europe?
Hi Kirsten, we have used Genoscreen and Ecogenics for our microsats so far and were very satisfied with them - they have a stepwise pricing system, allowing you to get products at every stage of the process, so for example, you could get the full library they can obtain, and then do the polymorphy check for yourself.
Systematic infanticide of unrelated young has been reported in several animal taxa. Particular attention has been given to carnivores and primates, where infanticide is a sexually selected strategy of males to gain increased access to female mating partners. Cannibals must ensure avoiding their own offspring and targeting only unrelated young. Therefore, decision rules are needed to mediate parental and cannibalistic behaviour. Here we show experimentally that male poison frogs adjust their parental responses – care or infanticide – towards unrelated clutches according to their territorial status. Male frogs followed the simple rule ‘care for any clutch’ inside their territory, but immediately switched to cannibalism when establishing a new territory. This demonstrates that simple cognitive rules can mediate complex behaviours such as parental care, and that care and cannibalism are antagonistically linked. Non-parental infanticide is mediated by territorial cues and presumably serves to prevent misdirected care in this poison frog. Our results thus prompt a re-consideration of evolutionary and causal aspects of parental decision making, by suggesting that selective infanticide of unrelated young may generally become adaptive when the risks and costs of misdirected care are high.
Acoustic species recognition in anurans depends on spectral and temporal characteristics of the advertisement call. the recognition space of a species is shaped by the likelihood of heterospecific acoustic interference. the dendrobatid frogs Allobates talamancae (cOpe, 1875) and Silverstoneia flotator (dunn, 1931) occur syntopi-cally in southwest costa rica. A previous study showed that these two species avoid acoustic interference by spectral stratification. In this study, the role of the temporal call structure in the advertisement call of A. talamancae was analyzed, in particular the internote-interval duration in providing species specific temporal cues. In playback trials, artificial advertisement calls with internote-intervals deviating up to ± 90 % from the population mean internote-interval were broadcast to vocally active territorial males. the phonotactic reactions of the males indicated that, unlike in closely related species, internote-interval duration is not a call property essential for species recognition in A. talamancae. however, temporal call structure may be used for species recognition when the likelihood of het-erospecific interference is high. Also, the close-encounter courtship call of male A. talamancae is described.
Question - Can anyone identify these frogs / Amphibians from Corcovado NP (Costa Rica)?
Sorry for the late reply, the email you used is not my most recent one and hardly checked. I agree with L. savagei, which basically is the split-off and newly described northern form of L. pentadactylus.
For the second picture S. sordida seems to be not a too bad guess - night colouration, as they look strikingly different during the day, and can also be highly variable. This is mainly based on proportions and shape of the snout and estimated size (as far as this is possible from the leaf). However, I have no identification literature available right now, and one would probably need more information (location, time, call) or even the specimen at hand for a good identification. I am not an expert on the Costa Rican herpetofauna, and the booklet from 2004 is mainly based on the book of Savage - I am more familiar with the Guiana Shield and Northern Brazil.
Figure S1: Sketch of the zoo of Vienna (‘Tiergarten Schönbrunn’). Figure S2: Division of the zoo into an evenly spaced hexagonal grid (grid sites) used to assess space use of crows. Figure S3: Maps generated in QGIS, to identify the number of foraging sites (a) and grid sites (b) individual crows were sighted in, respectively. Table S1: Frequency distribution of behavioural responses to coping style tests by all crows considered in the paper (n = 36).
While personality-dependent dispersal is well studied, local space use has received surprisingly little attention in this context, despite the multiple consequences on survival and fitness. Regarding the coping style of individuals , recent studies on personality-dependent space use within a habitat indicate that 'proactive' individuals are wider ranging than 'reactive' ones. However, such studies are still scarce and cover limited taxonomic diversity, and thus, more research is needed to explore whether this pattern generalises across species. We examined the link between coping style and space use in a population of crows (Corvus corone) freely inhabiting the urban zoo of Vienna, Austria. We used a binary docility rating (struggle during handling vs. no struggle) and a tonic immobility test to quantify individual coping style. Individual space use was quantified as the number of different sites at which each crow was observed, and we controlled for different number of sightings per individual by creating a space use index. Only the binary docility rating showed repeatability over time, and significantly predicted space use. In contrast to previous studies, we found that reactive crows (no struggle during handling) showed wider ranging space use within the study site than proactive individuals (who struggled during handling). The discrepancy from previous results suggests that the relationship between behavioural type and space use may vary between species, potentially reflecting differences in socioecology.
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.
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.
Reproductive skew, the uneven distribution of reproductive success among individuals, is a common feature of many animal populations. Several scenarios have been proposed to favour either high or low levels of reproductive skew. Particularly a male-biased operational sex ratio and the asynchronous arrival of females is expected to cause high variation in reproductive success among males. Recently it has been suggested that the type of benefits provided by males (fixed vs. dilutable) could also strongly impact individual mating patterns, and thereby affecting reproductive skew. We tested this hypothesis in Hyalinobatrachium valerioi, a Neotropical glass frog with prolonged breeding and paternal care. We monitored and genetically sampled a natural population in southwestern Costa Rica during the breeding season in 2012 and performed parentage analysis of adult frogs and tadpoles to investigate individual mating frequencies, possible mating preferences, and estimate reproductive skew in males and females. We identified a polygamous mating system, where high proportions of males (69 %) and females (94 %) reproduced successfully. The variance in male mating success could largely be attributed to differences in time spent calling at the reproductive site, but not to body size or relatedness. Female H. valerioi were not choosy and mated indiscriminately with available males. Our findings support the hypothesis that dilutable male benefits - such as parental care - can favour female polyandry and maintain low levels of reproductive skew among males within a population, even in the presence of direct male-male competition and a highly male-biased operational sex ratio. We hypothesize that low male reproductive skew might be a general characteristic in prolonged breeders with paternal care.
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.
Spreading reproduction across time or space can optimize fitness by minimizing the risks for offspring survival in varying and unpredictable environments. Poison frogs (Dendrobatidae) are characterized by complex spatial and reproductive behaviour, such as territoriality, prolonged courtship and parental care. The partitioning of larvae from terrestrial clutches across several water bodies is mainly known from species with carnivorous tadpoles that allocate their tadpoles in very small pools, where limited food availability is accompanied by an increased risk of cannibalism. However, little is known about the deposition behaviour of non-carnivorous species that use medium-sized to large pools. In the present study, we investigated whether the Neotropical poison frog Allobates femoralis exhibits brood-partitioning behaviour when males transport tadpoles 3 weeks after oviposition. We sampled 30 artificial water bodies for tadpoles, which we genotyped at seven highly polymorphic microsatellite loci. Based on the reconstructed pedigree, we show that A. femoralis males distribute larvae of single and of successive clutches across several water bodies. The number of pools used was significantly associated with the number of clutches per male. Ninety-three percent of the males that were assigned to more than one clutch spread their tadpoles across several water bodies. Given the highly variable and unpredictable biotic and abiotic conditions in tropical rainforest, at the spatial scale of the study species’ behaviour, we interpret this behaviour as bet-hedging to improve offspring survival.
“Ecosystem engineering” describes habitat alteration by an organism that affects another organism; such nontrophic interactions between organisms are a current focus in ecological research. Our study quantifies the actual impact an ecosystem engineer can have on another species by using a previously identified model system—peccaries and rainforest frogs. In a 4-year experiment, we simulated the impact of peccaries on a population of Allobates femoralis (Dendrobatidae) by installing an array of artificial pools to mimic a forest patch modified by peccaries. The data were analyzed using a gradual before-after control-impact (gBACI) model. Following the supplementation, population size almost doubled as a result of increased autochthonous recruitment driven by a higher per-capita reproduction of males and a higher proportion of reproducing females. The effect was evenly distributed across the population. The differential response of males and females reflects the reproductive behavior of A. femoralis, as only the males use the aquatic sites for tadpole deposition. Our study shows that management and conservation must consider nontrophic relationships and that human “ecosystem engineering” can play a vital role in efforts against the “global amphibian decline.”
Question - Does anyone know of a user friendly software for photo/pattern recognition of individual animals?
Wild-ID, which is around since ~2010, should work with the patterns of your frogs. We use it successfully with the dorsal patterns of Fire Salamanders (Salamandra salamandra) and the ventral patters of poison frogs (Allobates femoralis).
For animals with spatially complex behaviours at relatively small scales, the resolution of a global positioning system (GPS) receiver location is often below the resolution needed to correctly map animals’ spatial behaviour. Natural conditions such as canopy cover, canyons or clouds can further degrade GPS receiver reception. Here we present a detailed, high-resolution map of a 4.6 ha Neotropical river island and a 8.3 ha mainland plot with the location of every tree >5 cm DBH and all structures on the forest floor, which are relevant to our study species, the territorial frog Allobates femoralis (Dendrobatidae). The map was derived using distance- and compass-based survey techniques, rooted on dGPS reference points, and incorporates altitudinal information based on a LiDAR survey of the area.
Reliably marking larvae and re-identifying them after metamorphosis is a challenge that has hampered studies on recruitment, dispersal, migration, and survivorship of amphibians for a long time, since conventional tags are not reliably retained through metamorphosis. Molecular methods allow unique genetic fingerprints to be established for individuals. Although microsatellite markers have successfully been applied in mark-recapture studies on several animal species, they have never been previously used in amphibians to follow individuals across different life cycle stages. Here, we evaluate microsatellites for genetic across-stages mark-recapture studies in amphibians and test the suitability of available software packages for genotype matching. We sampled tadpoles of the dendrobatid frog Allobates femoralis, which we introduced on a river island in the Nature Reserve 'Les Nouragues' in French Guiana. In two subsequent recapture sessions we searched for surviving juveniles and adults, respectively. All individuals were genotyped at 14 highly variable microsatellite loci, which yielded unique genetic fingerprints for all individuals. We found large differences in the identification success of the programs tested. The pairwise-relatedness based approach, conducted with the programs KINGROUP or ML-Relate, performed best with our dataset. Matching ventral patterns of juveniles and adult individuals acted as a control for the reliability of the genetic identification. Our results demonstrate that microsatellite markers are a highly powerful tool for studying amphibian populations on an individual basis. The ability to individually track amphibian tadpoles throughout metamorphosis until adulthood will be of substantial value for future studies on amphibian population ecology and evolution. This article is protected by copyright. All rights reserved.
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.
Here we document the development of thirteen novel microsatellite markers for the reticulated glass frog Hyalinobatrachium valerioi (Centrolenidae). Nine of those markers were polymorphic and contained between 4 and 34 alleles per locus (mean = 20.3) in 138 individuals (91 males, 47 females) from the field site 'La Gamba', Costa Rica. Average observed heterozygosity was 0.76. Two loci (Hyval19 and Hyval21) significantly deviated from Hardy-Weinberg equilibrium. We did not find evidence for linkage disequilibrium among any of the loci. These markers will serve to identify the genetic mating system in H. valerioi, investigate gene flow between local populations, and reconstruct parent-offspring relationships for studies on individual mating and reproductive success. Therefore, these markers will serve to answer a wide range of scientific questions in conservation, behavioural ecology, and also evolutionary biology.
Introduction 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. Results 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. Conclusions 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.
In anurans, vocalization is the most prominent form of communication. Unique acoustic properties are used to enable species discrimination and to avoid mismating. Syntopic, vocally co-active frog species differentiate each other acoustically by using advertisement calls with different temporal and spectral properties. In territorial frogs, playbacks - mimicking conspecific or heterospecific territory intruders - are a powerful tool to test specific parameters of the acoustic recognition space. This paper describes the natural call properties of the syntopic and acoustically co-active dendrobatoid frogs Allobates talamancae (COPE, 1875) and Silverstoneia flotator (DUNN, 1931). In playback field experiments, spectrally manipulated but temporally unchanged advertisement calls of A. talamancae were used to analyze the males' recognition range against spectral variation. The call of A. talamancae exhibits a steep upward frequency sweep from 3.5 kHz to 5.0 kHz with a mean frequency of 4.2 kHz. Silverstoneia flotator calls with a frequency sweep from 5.2 kHz to 6.6 kHz around an average frequency of 6.1 kHz. Thus, the calls of both species do not overlap in the spectral domain. Broadcasting synthetically generated pure tone calls with the species' temporal properties to male A. talamancae evoked phonotactic responses over a wide range of frequencies around the population mean. Calls with frequencies below the population mean evoked significantly more response than calls with frequencies above the mean. The authors interpret the observed asymmetry in the response range of A. talamancae as a mechanism to avoid energy loss that would result from aggressive reactions to advertisement calls of S. flotator, which occurs sympatrically and is vocally co-active.
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.
Question - Has anyone used remote cameras for determining population density of mammals?
Here we document the development of seven novel polymorphic microsatellite markers for the brilliantthighed 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).
Dendrobatidae (dart-poison frogs) exhibit some of the most complex spa-tial behaviors among amphibians, such as territoriality and tadpole trans-port 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 lack-ing, and the underlying orientation mechanisms are unknown. We con-ducted a field translocation experiment to test whether male Allobates femoralis, a dendrobatid frog with paternal extra-territorial tadpole trans-port, 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 mecha-nisms involved and selective forces that could have shaped this strong homing ability.
The adaptive significance of sequential polyandry is a challenging question in evolutionary and behavioral biology. Costs and benefits of different mating patterns are shaped by the spatial distribution of individuals and by genetic parameters such as the pairwise relatedness between potential mating partners. Thus, females should become less choosy as costs of mating and searching for mates increase. We used parentage assignments to investigate spatial and genetic patterns of mating across a natural population of the Neotropical frog Allobates femoralis, a species characterized by male territoriality and care and female iteroparity. There was no correlation between genetic and spatial distances between adult individuals across the population. In 72% of cases, females mated with males available within a radius of 20 m. Mean pairwise relatedness coefficients of successful reproducers did not differ from random mating but had a lower variance than expected by chance, suggesting maximal reproductive output at intermediate genetic divergence. We also found evidence for selection in favor of more heterozygous individuals between the embryo and adult stage. The level of sequential polyandry significantly increased with the number of spatially available males. Females that had more candidate males also produced more adult progeny. We hypothesize that the benefits associated with female multiple mating outweigh the costs of in- and outbreeding depression, and consequently precluded the evolution of 'choosy' mate selection in this species.
While field and laboratory based studies have provided significant insights into the parental care and courtship behaviour of dendrobatoid frogs, a comprehensive assessment of their genetic mating systems and population genetic parameters has been precluded because of the lack of highly variable DNA markers. Here we document the development of nine novel polymorphic microsatellite markers for the dyeing poison frog Dendrobates tinctorius (Dendrobatidae). We found between three and 16 alleles per locus in 60 individuals (30 males, 30 females) from the field site Saut Pararé, French Guiana, with an average observed heterozygosity of 0.75. None of the loci deviated significantly from Hardy-Weinberg equilibrium or showed linkage disequilibrium. We also report successful cross-species amplification of the nine markers in two other dendrobatoid species (Allobates femoralis and Oophaga pumilio). These markers have the potential to aid in determining the genetic structure of local populations, identifying small-scale phylogenies such as parent-offspring relationships and will allow for cross-species comparisons within dendrobatoid species. Therefore, these markers can be applied to a wide range of scientific fields, such as conservation, behavioural ecology and evolutionary biology.
Example for the HRT-LSCV estimator. 95% (black area) and 50%-isoclines (grey area) of the HRT-LSCV estimator of the irregular virtual territory with increasing numbers of equiangular trials, based on all equiangular subsets that include the trials towards direction 0°. (TIF)
Average values of the different area estimators for equiangular trial-subsets in virtual territories. A) ellipse, B) star, C) triangle, D) angle, E) circle, F) irregular; horizontal grey line indicates ‘true’ absolute territory size; area in arbitrary units. (TIF)
Example for the detailed hull estimator. Detailed hull of the Central points (grey area) and outer points (black area) of the irregular virtual territory with increasing numbers of equiangular trials, based on all equiangular subsets that include the trials towards direction 0°. (TIF)
Example of the LoCoH estimator. LoCoH of the irregular virtual territory with increasing numbers of equiangular trials, based on all equiangular subsets that include the trials towards direction 0°; areas of stepwise increasing 5% isoclines in incremental shades of grey. (TIF)
Territoriality is a widespread behaviour in animals and its analysis is crucial in several areas of behavioural, ecological and evolutionary research. Commonly, territory size is assessed through territory mapping and the application of simple area estimators such as minimum convex polygons. In the present study we demonstrate that territory size can be determined adequately with an active approach through intrusion experiments, a technique that is commonly used in behavioural research in other contexts. Tests with simulated data indicate that a minimum of twelve trials needs to be performed to establish reliable orders of relative territory size. To estimate absolute territory size, detailed hull techniques are most appropriate when analyzing point patterns of intrusion experiments, while the local convex hull estimator enables the construction of internal utilization distributions based on such point patterns. Additionally we suggest a 'stretch the centre' approach to emphasize the actual process of intrusion experiments in the construction of internal utilization distributions. To demonstrate the utility of the method, we apply all findings from the simulations to data from fieldwork with the model species Allobates femoralis, a territorial aromobatid frog from the lowland rainforest of French Guiana.
Our knowledge about genetic mating systems and the underlying causes for and consequences of variation in reproductive success has substantially improved in recent years. When linked to longitudinal population studies, cross-generational pedigrees across wild populations can help answer a wide suite of questions in ecology and evolutionary biology. We used microsatellite markers and exhaustive sampling of two successive adult generations to obtain population-wide estimates of individual reproductive output of males and females in a natural population of the Neotropical frog Allobates femoralis (Aromobatidae), a pan-Amazonian species that features prolonged iteroparous breeding, male territoriality and male parental care. Parentage analysis revealed a polygynandrous mating system in which high proportions of males (35.5%) and females (56.0%) produced progeny that survived until adulthood. Despite contrasting reproductive strategies, successfully reproducing males and females had similar numbers of mating partners that sired the adult progeny (both sexes: median 2; range 1-6); the numbers of their offspring that reached adulthood were also similar (both sexes: median 2; range 1-8). Measures of reproductive skew indicate selection on males only for their opportunity to breed. Reproductive success was significantly higher in territorial than in nonterritorial males, but unrelated to territory size in males or to body size in both sexes. We hypothesize that female polyandry in this species has evolved because of enhanced offspring survival when paternal care is allocated to multiple partners.
Toe-clipping is a standard method for marking and tissue sampling in amphibians, and in most adult anurans such marks are permanent. Here we document the consistent regeneration of toes in the aromobatid frog Allobates femoralis during a three-year population study. The emergence of new toe discs was observed after about two months. After one year the regrown toes had recovered to 65.6%/63.8% (males/females) of the size of unclipped toes and after two years they had attained 74.0%/69.0%. Whereas toe discs before amputation were white dorsally, all but one regenerated toe discs were dark. We did not detect any malformations or infections of the digits. Recapture rates of toe-clipped individuals were indiscernible from those of a nearby population where no toe clips were taken. We discuss a possible link between toe regeneration ability and life-history attributes.
Subsumed under the vernacular name "poison frogs", the superfamily Dendrobatoidea contains the "non-poisonous poison frogs" in the family Aromobatidae and the "true poison frogs" in the family Dendrobatidae (Grant et al., 2006). While the latter regularly feature bright, aposematic colouration and potent skin toxins, members of the Aromobatidae are usually cryptically coloured and rely on camouflage and rapid escape behaviour as anti-predator measures (Cooper, Caldwell and Vitt, 2009). Despite intensive research on various aspects of dendrobatoid biology, little information is available on natural predators of this taxon (cf. Darst and Cummings, 2006; Saporito et al., 2007; Cooper, Caldwell and Vitt, 2009; Noonan and Comeault, 2009). Allobates femoralis is a semi-cryptic pan-Amazonian aromobatid frog (Amézquita et al., 2009) and possesses, at the most, only traces of skin toxins of the potent alkaloid classes know from dendrobatids (Daly, Myers and Whittaker, 1987). However, the species was found to be a Batesian mimic of poisonous species of the dendrobatid genus Epipedobates (Darst and Cummings, 2006), including E. hahneli, which is syntopic with A. femoralis at the observation site in French Guiana (Lescure and Marty, 2000; Born and Gaucher, 2001). Additionally, the skin Herpetology Notes, volume 3: 301-304 (2010) (published online on 22 November 2010)
We studied movement and site fidelity of males and females of the territorial frog Allobates femoralis (Aromobatidae) in a population in the Nature Reserve “Les Nouragues” in French Guiana, South America. Observations during 3months in 2006 ascertained intra-seasonal site fidelity for males and females. Males actively defend large multi-purpose territories whereas females retreat to small resting sites from where they commute to neighbouring males for courtship and mating. Female short-term movement corroborates the previous assumption of a polygynous or promiscuous resource-defence mating system. Year-to-year recaptures from 2005 until 2008 revealed distinct patterns of inter-annual movement for males and regional site fidelity for females. Males abandon their territories and have to re-negotiate them when reproduction starts again at the end of the dry season. Females are not subject to intra- or inter-sexual territorial competition and as a result move significantly less between reproductive seasons than males. Male long-term movement reflects spatial structure and prevailing social interactions and is a reliable indicator for tadpole deposition sites. The combined effects of intra- and inter-seasonal movement promote the diversity of mates for both sexes.
Phonotactic approaches by 17 male Allobates femoralis were videotaped and analysed in terms of spatial and temporal patterns to assess this species' ability to localise sound. Jump angles of consecutive jumps and the straightness of paths were measured to quantify the ac-curacy of approach. The effect of interbout intervals on phonotactic approach was examined by comparing movement parameters of two tests, using a standard call with interbout inter-vals, and a continuous call without interbout intervals. Phonotactic approach occurred almost exclusively during calling bouts. Interbout intervals interrupted movement and did not alter the accuracy of approach. Our results suggest that only the calling bouts, but not the silent in-terbout intervals, play a crucial role for male phonotaxis in this species. Furthermore, anuran phonotactic approach is not strictly axis-alternated and, thus, not appropriately described by the generally used term 'zig-zagging'.