The Homing Frog: High Homing Performance in a Territorial Dendrobatid Frog Allobates femoralis (Dendrobatidae)

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.     

Acoustic and Morphological Differentiation in the Frog Allobates femoralis: Relationships with the Upper Madeira River and Other Potential Geological Barriers

We studied patterns of call acoustics and external morphological differentiation in populations of the dart-poison frog Allobates femoralis occurring in forested areas along a 250-km stretch of the upper Madeira River, Brazil. Multivariate analyses of variance using principal components representing shared acoustic and morphological parameters distinguished three groups in relation to call structure and external morphology: (1) populations belonging to a two-note call morphotype; (2) populations with four-note calls inhabiting the left riverbank; and (3) populations with four-note calls inhabiting the right riverbank. Our results report a case of Amazonian anuran diversity hidden by current taxonomy and provide evidence for the upper Madeira River being a boundary between distinct populations of A. femoralis , and suggest a new taxonomic interpretation for these groups. Samples that did not fit into the general differentiation pattern and the existence of a well-defined contact zone between two morphotypes on the left riverbank indicate that mechanisms complementary to river-barrier hypotheses are necessary to explain the phenotypic differentiation between populations. Our study shows that at least one anuran species shows congruence between population differentiation and separation by a large Amazonian river, as documented for birds and mammals. Conservation efforts should not consider the taxon now known as A. femoralis as a homogeneous entity. There is much within-taxon variability, which can be probably explained partly by the existence of cryptic species, partly by geological barriers and part of which currently has no obvious explanation.     

Masking interference and the evolution of the acoustic communication system in the Amazonian dendrobatid frog Allobates femoralis

The efficacy of communication relies on detection of species-specific signals against the background noise. Features affecting signal detection are thus expected to evolve under selective pressures represented by masking noise. Spectral partitioning between the auditory signals of co-occurring species has been interpreted as the outcome of the selective effects of masking interference. However, masking interference depends not only on signal's frequency but on receiver's range of frequency sensitivity; moreover, selection on signal frequency can be confounded by selection on body size, because these traits are often correlated. To know whether geographic variation in communication traits agrees with predictions about masking interference effects, we tested the hypothesis that variation in the male-male communication system of the Amazonian frog, Allobates femoralis, is correlated with the occurrence of a single species calling within an overlapping frequency range, Epipedobates trivittatus. We studied frogs at eight sites, four where both species co-occur and four where A. femoralis occurs but E. trivittatus does not. To study the sender component of the communication system of A. femoralis and to describe the use of the spectral range, we analyzed the signal's spectral features of all coactive species at each site. To study the receiver component, we derived frequency-response curves from playback experiments conducted on territorial males of A. femoralis under natural conditions. Most geographic variation in studied traits was correlated with either call frequency or with response frequency range. The occurrence of E. trivittatus significantly predicted narrower and asymmetric frequency-response curves in A. femoralis, without concomitant differences in the call or in body size. The number of acoustically coactive species did not significantly predict variation in any of the studied traits. Our results strongly support that the receiver but not the sender component of the communication system changed due to masking interference by a single species.     

Temporal and Geographic Variation in the Advertisement Call of the Booroolong Frog (Litoria booroolongensis: Anura: Hylidae)

The mechanisms that underlie sexual selection rely upon within‐ and among‐individual variability in the targeted traits. In this study, we examined variation in the advertisement call of the booroolong frog (Litoria booroolongensis) at several different levels: between populations, between breeding seasons in the same population, among males within a population, within males between nights and within males in a single calling bout. The call of L. booroolongensis has multiple notes with a pulsed structure. We detected considerable variation in advertisement call structure between breeding seasons and between populations. The measured call properties ranged from static to dynamic; however, most properties were intermediate between the criteria that have been traditionally used to define call traits as static or dynamic (≤5 and ≥12% respectively). We compared actual and relative repeatabilities and found that the temporal call properties associated with the structure of the note had the highest values, suggesting that these characters in particular may respond to selection. We argue that relative repeatabilities are a particularly useful measure of the potential for evolutionary response to selection as they account for an individual's relative performance during the period of assessment in an ever‐changing breeding arena.     

Conspicuousness,color resemblance,and toxicity in geographically diverging mimicry: The pan‐Amazonian frog Allobates femoralis

Predation risk is allegedly reduced in Batesian and Müllerian mimics, because their coloration resembles the conspicuous coloration of unpalatable prey. The efficacy of mimicry is thought to be affected by variation in the unpalatability of prey, the conspicuousness of the signals, and the visual system of predators that see them. Many frog species exhibit small colorful patches contrasting against an otherwise dark body. By measuring toxicity and color reflectance in a geographically variable frog species and the syntopic toxic species, we tested whether unpalatability was correlated with between‐species color resemblance and whether resemblance was highest for the most conspicuous components of coloration pattern. Heterospecific resemblance in colorful patches was highest between species at the same locality, but unrelated to concomitant variation in toxicity. Surprisingly, resemblance was lower for the conspicuous femoral patches compared to the inconspicuous dorsum. By building visual models, we further tested whether resemblance was affected by the visual system of model predators. As predicted, mimic‐model resemblance was higher under the visual system of simulated predators compared to no visual system at all. Our results indicate that femoral patches are aposematic signals and support a role of mimicry in driving phenotypic divergence or mimetic radiation between localities.     

Intrusion experiments to measure territory size: development of the method, tests through simulations, and application in the frog Allobates femoralis

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.     

Territoriality and Male Mating Success in the Dart-poison Frog,Epipedobates femoralis (Dendrobatidae,Anura)

The social and reproductive behaviour of the dart-poison frog, Epipedobates femoralis, was studied in Amazonian Peru for 14 months. Males defended territories with advertisement calls and, ultimately, fighting. Territory size ranged from 0.25 to 26 m² and was positively correlated with duration of residence and calling activity of the owner. Females were not territorial and were never attacked when approaching calling males. Males and females only mated once and females sampled calling males before mating. Male mating success was closely correlated with territory size and calling activity. No correlation was found between male body size and mating success. Territories provide residents with sufficient space for mate attraction and reproduction without interference from rivals. Since territory size is dependent on calling activity which involves high energetic costs, it is suggested that territory size reveals male quality.     

Calls,colours, shape,and genes: a multi‐trait approach to the study of geographic variation in the Amazonian frog Allobates femoralis

Evolutionary divergence in behavioural traits related to mating may represent the initial stage of speciation. Direct selective forces are usually invoked to explain divergence in mate‐recognition traits, often neglecting a role for neutral processes or concomitant differentiation in ecological traits. We adopted a multi‐trait approach to obtain a deeper understanding of the mechanisms behind allopatric divergence in the Amazonian frog, Allobates femoralis. We tested the null hypothesis that geographic distance between populations correlates with genetic and phenotypic divergence, and compared divergence between mate‐recognition (acoustic) and ecological (coloration, body‐shape) traits. We quantified geographic variation in 39 phenotypic traits and a mitochondrial DNA marker among 125 individuals representing eight populations. Geographic variation in acoustic traits was pronounced and tracked the spatial genetic variation, which appeared to be neutral. Thus, the evolution of acoustic traits tracked the shared history of the populations, which is unexpected for pan‐Amazonian taxa or for mate‐recognition traits. Divergence in coloration appeared uncorrelated with genetic distance, and might be partly attributed to local selective pressures, and perhaps to Batesian mimicry. Divergence in body‐shape traits was low. The results obtained depict a complex evolutionary scenario and emphasize the importance of considering multiple traits when disentangling the forces behind allopatric divergence. ©2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 826–838.     

基于功能域组分的蛋白质折叠类型识别

蛋白质空间结构研究是分子生物学、细胞生物学、生物化学以及药物设计等领域的重要课题.折叠类型反映了蛋白质核心结构的拓扑模式,对折叠类型的识别是蛋白质序列与结构关系研究的重要内容.选取LIFCA数据库中样本量较大的53种折叠类型,应用功能域组分方法进行折叠识别.将Astral 1.65中序列一致性小于95%的样本作为检验集,全库检验结果中平均敏感性为96.42%,特异性为99.91%,马修相关系数(MCC)为0.91,各项统计结果表明:功能域组分方法可以很好地应用在蛋白质折叠识别中,LIFCA相对简单的分类规则可以很好地集中蛋白质的大部分功能特性,反映了结构与功能的对应关系.     

The Consequences for Communication of Call Overlap in the Tungara Frog,a Neotropical Anuran with a Frequency-modulated Call

We presented male tungara frogs, Physalaemus pustulosus, with call-triggered computer-synthesized whines that either did or did not overlap the frogs' own frequency-modulated whines in time. When the stimulus was nonoverlapping, males added a high proportion of chuck notes to their calls. When the stimulus was overlapping, males responded with either no or only small increases in chucking. This suggests they have difficulty detecting whines while vocalizing. When female tungara frogs were given a choice between alternating whines and out-of-phase overlapping whines they did not discriminate. The result with males was similar to that previously obtained with species of frogs that have amplitude-modulated advertisement calls (Schwartz 1987a), the result with females was different. We discuss our findings in relation to peripheral processing of spectral and temporal information in the anuran auditory system.     

Advertisement Call Variation in the Golden Rocket Frog (Anomaloglossus beebei): Evidence for Individual Distinctiveness

Individual distinctiveness in acoustic signals can allow receivers to respond appropriately to different individuals. The aim of this research was to examine signal variation and to investigate the relative importance of different acoustic properties for coding individual distinctiveness in the advertisement calls of male golden rocket frogs (Anomaloglossus beebei). We examined patterns of within‐individual and among‐individual variability in 760 advertisement calls of 40 males as well as repeatability in 16 additional males that were recorded on two different occasions. We examined eight call properties, and all properties exhibited significant among‐individual variation and moderate to high repeatability across days. We employed discriminant function analysis to examine individual distinctiveness statistically. These analyses assigned 79% of calls to the correct individual. Fine temporal properties, including pulse duration, pulse rate, and pulse interval, as well as the spectral property of dominant frequency, contributed most toward discrimination among individuals. These results indicate that individual male golden rocket frogs can be distinguished statistically by their advertisement calls. We use these findings to evaluate results of previous playback studies in A. beebei and to generate testable predictions regarding the potential for specific call properties to function in mate selection and social recognition.     

Signal Redundancy and Receiver Permissiveness in Acoustic Mate Recognition by the Tungara Frog, Physalaemus pustulosus

The tungara frog has an advertisement call with two structurallyand functionally distinct components: the whine is both necessaryand sufficient for species recognition, and addition of chucksfurther enhances call attractiveness. Only the fundamental frequencyof the whine contributes to phonotaxis; the upper harmonicsplay no role. Furthermore, only a small portion of the whine,within the first 0–100 msec, is necessary to elicit phonotaxis;there is some redundancy since either the 0–50 msec orthe 50–100 msec portion elicits a response. Most of theremainder of the whine's fundamental further enhances call attractiveness.Only the amphibian papilla in the peripheral auditory systemis involved in decoding the whine. In stark contrast, severalchuck variants, which stimulate either the amphibian papillaor the basilar papilla, and white noise are as effective inenhancing call attractiveness as is the normal chuck, showingthat either peripheral end organ can be involved in the perceptionof a more attractive call. Thus there is greater receiver specificityfor decoding stimuli in interspecific mate choice, and greaterreceiver permissiveness for decoding stimuli in intraspecificmate choice; it appears that intraspecific mate choice can takeadvantage of a greater array of neural pathways for call decodingthan can interspecific mate choice.     

凹耳蛙及无尾两栖动物发声系统形态学研究进展

两栖动物是最早应用声讯进行雌雄识别、繁殖和防御的脊椎动物,其发声器官包括喉部器官和(或)声囊.近来的研究表明我国特有两栖动物--凹耳蛙不仅具有非常复杂的鸣叫特点,而且能发出超声音频.本文总结了有关凹耳蛙的生物学特点、无尾两栖动物发声器官的研究进展,指出凹耳蛙在无尾两栖动物发声器官的生态和进化形态学研究中的重要地位.     

Transdifferentiation of Adult Frog Iris in Retina or Lens by Exogeneous Influences

The mechanisms of transdifferentiation of iris epithelial cells of Rana temporaria (Anura) in culture depending on influences from different sources were studied. In terminally differentiated iris cells, the process of transdifferentiation is initiated by dedifferentiation. Melanosomes are shed from iris cells due to cell surface activity. After depigmentation, iris epithelial cells become capable of proliferating and competent to react to the influences of various exogenous factors. Under the influence of retinal factors secreted by lentectomized tadpole eyes, both dorsal and ventral irises are converted to neural retina. Under the influence of factors from eye vesicles, the irises are converted to neural retina as well. Similar results were obtained in transfilter experiments, in which a 3-day period of transfilter interaction between the irises and eye vesicles ensured depigmentation of the iris followed by transdifferentiation into complete NR with visual receptor. Lentoid formation occurred under the influence of adult frog lens epithelium. Immunofluorescent analysis confirmed the lens nature of the lentoids. In control experiments under the conditions of the tadpole eye orbit, in which programming influences were absent, iris epithelial cells remained unaffected.
The problem of true cell-reprogramming to new differentiation in contrast to expression of inherent properties of the iris epithelial cells is discussed.     

Female Preferences for Call Traits and Male Mating Success in the Neotropical Frog Physalaemus enesefae

Female preferences for male call traits may affect male mating success and the evolution of exaggerated secondary sexual traits. We used phonotaxis experiments to examine female preferences in the frog Physalaemus enesefae in relation to variation in male call duration, dominant frequency, intercall interval and amplitude (dB SPL). Females preferred long calls, low and average dominant frequency calls, short intercall intervals and more intense calls. We compared the patterns of female preferences with those of acoustic variation among males to test the prediction that properties with low within‐male variation are associated with stabilizing or weakly directional female preferences, whereas properties with high within‐male variation are associated with directional preferences. Females had weakly directional preferences for the dominant frequency of the call and strongly directional preferences for call duration and call rate. We also determined whether the temporal relationship between calls influenced preferences based on the dominant frequency of the call. Preferences for low‐frequency over high‐frequency calls disappeared when calls partially overlapped. Females preferred the leading call regardless of its dominant frequency. We also investigated mating patterns in the field. There was size‐assortative mating, as male and female body sizes snout‐vent length (SVL) were positively correlated. In addition, differences in the frequency distributions of body length (SVL) between mated and unmated males approached significance; lower SVL classes were underrepresented among mated males. These patterns may reflect female preferences for lower dominant frequency calls, as there is a negative correlation between male mass and the dominant frequency of the call.     

The Two Endocytic Pathways Mediated by the Carbohydrate Recognition Domain and Regulated by the Collagen-like Domain of Galectin-3 in Vascular Endothelial Cells

Galectin-3 plays an important role in endothelial morphogenesis and angiogenesis. We investigated the endocytosis of galectin-3 in human vascular endothelial cells and showed that galectin-3 could associate with and internalized into the cells in a carbohydrate-dependent manner. Our work also revealed that galectin-3 was transported to the early/recycling endosomes and then partitioned into two routes – recycling back to the plasma membrane or targeting to the late endosomes/lysosomes. Various N- and C-terminal truncated forms of galectin-3 were constructed and compared with the full-length protein. These comparisons showed that the carbohydrate-recognition domain of galectin-3 was required for galectin-3 binding and endocytosis. The N-terminal half of the protein, which comprises the N-terminal leader domain and the collagen-like internal repeating domain, could not mediate binding and endocytosis alone. The collagen-like domain, although it was largely irrelevant to galectin-3 trafficking to the early/recycling endosomes, was required for targeting galectin-3 to the late endosomes/lysosomes. In contrast, the leader domain was irrelevant to both binding and intracellular trafficking. The data presented in this study correlate well with different cellular behaviors induced by the full-length and the truncated galectin-3 and provide an alternative way of understanding its angiogenic mechanisms.     

Matching and Symmetry in the Frequency Recognition Curve of the Poison Frog Epipedobates trivittatus

In territorial species, males use signals to advertise territory ownership to other males. In species with acoustic communication, masking interference by heterospecific signals may impede male–male communication and affect the reproductive success of males. Frogs are thought to minimize masking interference by using species‐specific frequency channels for communication. For this strategy to work, a frequency match is expected between the advertisement call and the auditory sensitivity. A previous field study on the Amazonian frog Epipedobates femoralis supported this prediction, but also revealed an asymmetric decrease in the probability of male reaction towards synthetic calls. That males of E. femoralis reacted less towards low‐frequency (compared with high‐frequency) calls was interpreted as a mechanism that reduces masking interference by E. trivittatus, a species calling within a lower, partially overlapping, frequency range. If this hypothesis holds, then males of E. trivittatus should exhibit the opposite asymmetry pattern, i.e. react less towards high‐frequency (compared with low‐frequency) calls. We tested this prediction by conducting 25 playback experiments on 22 males of E. trivittatus. Male phonotactic reaction towards synthetic calls of various frequency values was evaluated as a binary variable (the male either approached or not the loudspeaker), by measuring the latency until first jump, and by calculating the linear approaching speed. As in E. femoralis, the maximum probability of positive reaction was matched to the call frequency. Against our expectations, the response curve was symmetric. We discuss whether these results reflect a lack of selective pressures, or a compromise between natural selection and physiological constraints on the shape of the frequency recognition curves.