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Allobates femoralis External morphology. Description based on nine tadpoles between Stages 34 and 38 (LCS 458, 577, 706). Total length 29.1 ± 1.3 mm (mean ± 1 standard deviation SD; N = 4 tadpoles at Stages 36 and 37). Body oval in dorsal view and globular/depressed in lateral view (Fig. 4A, B). Snout rounded in dorsal view and truncate in lateral view. Eyes small, dorsally positioned and dorsolaterally directed. Nostrils small, circular, dorsally positioned closer to snout than to eyes, with opening laterally directed, without a projection on marginal rim. Oral disc (Fig. 4C) anteroventral, laterally emarginate; marginal papillae conical, uniseriate, with a wide dorsal gap. Submarginal papillae absent. LTRF 2(2)/3(1); A1 and A2 of the same length; P3 slightly shorter than P1 and P2. Jaw sheaths narrow, finely serrate; the anterior jaw sheath arch-shaped, posterior jaw sheath U-shaped. Spiracle single, sinistral, cylindrical, short and wide, posterodorsally directed, opening on the middle third of the body with the centripetal wall fused to the body wall, and longer than the external wall. Vent tube long, dextral, fused to the ventral fin, with dextral opening. Caudal musculature of moderate width; in lateral view gradually tapering to a pointed tip. Dorsal fin shallow, convex and originating at the tail-body junction; ventral fin shallow and parallel to the ventral margin of caudal musculature. Tail tip pointed. Lateral lines visible. Colour. In preservative, body brown or grayish brown, belly transparent, digestive tract visible; caudal musculature creamy colored and tail fins translucent; both caudal musculature and fins covered with melanophores forming many brown or grayish brown blotches. In life, dorsum grayish brown, lateral of the body with chromatophores forming small silvery spots, venter translucent; caudal musculature pale brown with melanophores forming blotches, tail fins translucent (Fig. 4D). Variation. LTRF 2(2)/3(1) from Stage 32 onwards. At Stage 27 LTRF ranges from 1/2 to 2/2 to 2(2)/3(1). Metamorphs. Dorsum gray to black with a light brown dorsolateral line barely reaching the end of the body; belly with irregular dark markings; orange patch on the outside of the thigh and a yellow patch on the base of the anterior arm (Fig. 4E). Natural history. Eggs are deposited in the forest floor between fallen leaves. Clutches contain from 8 to 17 pigmented eggs (Lima et al. 2012). Tadpoles at Stage 27 are carried on the back of the males (Lima et al. 2012) and rarely females (Ringler et al. 2015) to small, temporary, isolated or streamside ponds and puddles in terra-firme forests and forest edge (this study). Larvae are found in all months of the year. Larvae are benthic and camouflaged against the substrate. Larvae consume detritus (Weygoldt 1980) and anuran eggs (Magnusson & Hero 1991). In experiments larvae were found to be preyed upon by dragonfly larvae and fish (Gascon 1992a). Comments. Tadpoles of A. femoralis were previously described by Duellman (1978) from Ecuador, by Hero (1990) from Central Amazonia, Brazil and by Duellman (2005) from Peru. Tadpoles described herein differ from those described by Duellman (1978) by presenting LTRF 2(2)/3; and from those described by Duellman (2005) by presenting dorsal fin originating on the tail and a rounded tail tip (although Fig. 13.2E in Duellman 2005 shows a tadpole with a pointed tail tip). There are no morphological differences between tadpoles herein characterized and those from Central Amazonia, Brazil, illustrated in Hero (1990)., Published as part of Schiesari, Luis, Rossa-Feres, Denise De Cerqueira, Menin, Marcelo & Hödl, Walter, 2022, Tadpoles of Central Amazonia (Amphibia: Anura), pp. 1-149 in Zootaxa 5223 (1) on pages 24-25, DOI: 10.11646/zootaxa.5223.1.1, http://zenodo.org/record/7517957, {"references":["Lima, A. P., Magnusson, W. E., Menin, M., Erdtmann, L. K., Rodrigues, D. J., Keller, C. & H ˆ dl, W. (2012) Guia de Sapos da Reserva Adolpho Ducke, Amazonia Central / Guide to the frogs of Reserva Adolpho Ducke, Central Amazonia. 2 nd Edition. Editora INPA, Manaus, 187 pp.","Ringler, E., Pasukonis, A., Firch, W. T., Huber, L., H ˆ dl, W. & Ringler, M. (2015) Flexible compensation of uniparental care: female poison frogs take over when males disappear. Behavioral Ecology, 26, 1219 - 1225. https: // doi. org / 10.1093 / beheco / arv 069","Weygoldt, P. (1980) Zur Fortpflanzungsbiologie von Phyllobates femoralis (Boulenger) im Terrarium (Amphibia: Salientia: Dendrobatidae). Salamandra, 16, 215 - 226.","Magnusson, W. E. & Hero, J-M. (1991) Predation and the evolution of complex oviposition behaviour in Amazon rainforest frogs. Oecologia, 86, 310 - 318. https: // doi. org / 10.1007 / BF 00317595","Gascon, C. (1992 a) Aquatic predators and tadpole prey in central Amazonia: field data and experimental manipulations. Ecology, 73, 971 - 980. https: // doi. org / 10.2307 / 1940173","Duellman, W. E. (1978) The biology of an Equatorial herpetofauna of Amazonian Ecuador. Miscellaneous Publications Museum of Natural History University of Kansas, 65, 1 - 352.","Duellman, W. E. (2005) Cusco Amazonico - the lives of amphibians and reptiles in an Amazonian rainforest. Cornell University Press, Ithaca, New York, 433 pp."]}

Biogeographic barriers such as rivers have been shown to shape spatial patterns of biodiversity in the Amazon basin, yet relatively little is known about the distribution of genetic variation across continuous rainforest. Here, we characterize the genetic structure of the brilliant-thighed poison frog (Allobates femoralis) across an 880-km-long transect along the Purus-Madeira interfluve south of the Amazon river, based on 64 individuals genotyped at 7609 single-nucleotide polymorphism (SNP) loci. A population tree and clustering analyses revealed 4 distinct genetic groups, one of which was strongly divergent. These genetic groups were concomitant with femoral spot coloration differences, which was intermediate within a zone of admixture between two of the groups. The location of these genetic groups did not consistently correspond to current ecological transitions between major forest types. A multimodel approach to quantify the relative influence of isolation-by-geographic distance (IBD) and isolation-by-environmental resistance (IBR) nevertheless revealed that, in addition to a strong signal of IBD, spatial genetic differentiation was explained by IBR primarily linked to dry season intensity (r2 = 8.4%) and canopy cover (r2 = 6.4%). We show significant phylogenetic divergence in the absence of obvious biogeographical barriers and that finer-scaled measures of genetic structure are associated with environmental variables also known to predict the density of A. femoralis.

For animals to survive until reproduction, it is crucial that juveniles successfully detect potential predators and respond with appropriate behavior. The recognition of cues originating from predators can be innate or learned. Cues of various modalities might be used alone or in multi-modal combinations to detect and distinguish predators but studies investigating multi-modal integration in predator avoidance are scarce. Here, we used wild, naive tadpoles of the Neotropical poison frog Allobates femoralis ( Boulenger, 1884) to test their reaction to cues with two modalities from two different sympatrically occurring potential predators: heterospecific predatory Dendrobates tinctorius tadpoles and dragonfly larvae. We presented A. femoralis tadpoles with olfactory or visual cues, or a combination of the two, and compared their reaction to a water control in a between-individual design. In our trials, A. femoralis tadpoles reacted to multi-modal stimuli (a combination of visual and chemical information) originating from dragonfly larvae with avoidance but showed no reaction to uni-modal cues or cues from heterospecific tadpoles. In addition, visual cues from conspecifics increased swimming activity while cues from predators had no effect on tadpole activity. Our results show that A. femoralis tadpoles can innately recognize some predators and probably need both visual and chemical information to effectively avoid them. This is the first study looking at anti-predator behavior in poison frog tadpoles. We discuss how parental care might influence the expression of predator avoidance responses in tadpoles., Summary: Poison frog tadpoles innately recognize dragonfly larvae as dangerous using a combination of visual and olfactory cues.

Breeding sites are often a limited and ephemeral resource for rainforest frogs. This resource limitation has driven the evolution of diverse reproductive strategies that increase offspring survival. For example, poison frogs shuttle their tadpoles from terrestrial clutches to aquatic rearing sites, using various cues to assess pool suitability. Yet, how frogs find new pools is unknown. We tested the role of odor cues in the process of finding tadpole deposition sites by the poison frog Allobates femoralis. We created 60 artificial pools grouped into three conditions: stagnant water, tadpole water and clean water control. Fifteen pools were discovered within 6 days, with more tadpoles and more frogs directly observed at pools with stagnant odor cues. Our findings suggest that frogs use odor cues associated with stagnant water for the initial discovery of new breeding pools. These cues may be good indicators of pool stability and increased likelihood of tadpole survival., Summary: Amphibians rely on water for reproduction; however, very little is known on how amphibians find water bodies. Experiments in Allobates femoralis suggest that frogs use stagnant odor cues to find breeding pools.

Territorial behaviour 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 (e.g. testosterone) are involved in the modulation of territorial behaviour 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 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.

Abstract Most male frogs produce calls to attract females and repel rivals. The transmission of these calls can be affected by many acoustic and environmental characteristics, which can influence the detection and decoding of the signal by the receiver. Calling-perch height has a strong influence on sound propagation and acoustic spacing with neighboring males, but how frogs optimize their calling behavior in this context is poorly understood. In this study, we investigated if and how frogs can adjust the calling energy in the context of acoustic spacing. Our aim was to evaluate the relationship between calling-perch height, nearest-neighbor distance, and sound-pressure level in the brilliant-thighed poison frog Allobates femoralis. We found that frogs flexibly adjust the calling amplitude according to the calling-perch height without affecting the effectiveness signal propagation. Accompanying signal propagation experiments demonstrated that calls produced with lower amplitude from higher perches propagate similar to louder calls from the ground. Our results suggest an adjustment to the hypothesis of a general positive effect of calling-perch height on signal effectiveness, where highly territorial frogs adjust their calling behavior to reduce energy expenditure and optimize acoustic communication with conspecifics. Significance statement In acoustically communicating species, sound propagates better when broadcasted from elevated positions. However, callers may adjust their calling behavior to optimize the sound transmission under ecological constraints. By using a correlative and manipulative approach, we show in a poison frog model that males can adjust their calling amplitude according to the calling-perch height. We then discuss that this calling adjustment optimizes the acoustic spacing between conspecific males and reduces energy consumption.

El presente estudio describe la morfometría del testículo y la línea espermatogénica de especímenes adultos (N=8) de Allobates femoralis (Boulenger, 1883) colectados en la Estación Biológica Panguana (9°37'S 74°56'W), 250 msnm, 4 – 5 km rio arriba del Rio Pachitea, Distrito de Yuyapichis, provincia de Puerto Inca, Huánuco, Perú. Los anfibios (longitud 25,99±0,97 mm) fueron diseccionados y aislados los testículos con el propósito de obtener datos biométricos, posteriormente se realizaron cortes histológicos, coloreándose con hematoxilina y eosina; los estadios germinales observados fueron descritos y luego medidos con ayuda de un ocular micrométrico. La biometría obtenida de los testículos fue: eje mayor = 2,254 mm (DE = 0,282); eje menor = 1,343 mm (DE = 0,181); ancho = 0,971 mm (DE = 0,097); a nivel microscópico encontramos una capa albugínea (6,51±1,74 mì) constituida por tejido conectivo y músculo liso. Los túbulos seminíferos (162.56±47.61mì) están delimitados por una delgada capa de tejido conectivo. En relación a los aspectos reproductivos, se observó en A. femoralis que la espermatogenesis ocurre en los túbulos seminíferos donde los elementos celulares están organizados en espermatocistos. Cada cisto contiene células en el mismo estadio de desarrollo. La caracterización de cada tipo celular permitió la identificación de las células del linaje germinal: 1) Espermatogonias, son células aisladas o en grupos más voluminosas del linaje espermático (7,07±1,187 mì), tienen núcleo irregular, presenta granulaciones cromatínicas y se encuentran por lo general muy cerca de la pared tubular. 2) Espermatocito I, con tamaño menor que las espermatogonia (6,95±1,21mì), 3) Espermátides; redondeadas, con cromatina fina; a medida que avanzan en su desarrollo, éstas se elongan y se organizan en “atados” cuyas cabezas están sujetas entre si. 4). Los espermatozoides tienen forma alargada siendo su flagelo menos teñido, el núcleo es compactado y el citoplasma se reduce, están distribuidos hacia el lumen del túbulo seminífero. Se reporta por primera vez la descripción macroscópica y microscopia del testículo de A. femoralis para el Perú.

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.

Amezquita et al. (2017) recently concluded that species of the Allobates femoralis group are toxic to mice at levels equivalent to syntopic alkaloid-containing poison frogs, which they attributed to the presence of alkaloids in skin secretions. However, the chemical composition of skin secretions was not analyzed, and here we present additional data supporting the absence of alkaloids in skin secretions of the Allobates femoralis group. Instead, we suggest the observed toxicity was caused by the anesthetic benzocaine, which was applied to the buccal cavity to euthanize frogs prior to skin removal. We show that orally administered benzocaine is rapidly incorporated into the skin of species that sequester and do not sequester alkaloids, which casts doubt on the conclusion that Allobates femoralis group skin secretions are toxic and makes the results of experiments with alkaloid-containing species of Adelphobates and Ameerega uninterpretable. To prevent experimental errors and misinterpretations in studies of amphibian chemical defense, we encourage researchers to test the chemical composition of samples prior to experimentation, include all necessary controls to detect false positives, conduct small pilot studies for new methods, and consider the limitations of particular methods and their ability to address the intended research questions.

Predation risk is allegedly reduced in Batesian and Mullerian 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.

Allobates femoralis (Boulenger, 1884) TYPE LOCALITY. — Yurimaguas, Huallaga River, Loreto, Peru. DISTRIBUTION. — Throughout Amazonia. TAXONOMIC REMARKS. — This widespread species represents a species complex with noticeable differences in call, morphology, and genetics (Amézquita et al. 2009). The populations of the Guiana Shield display several mitochondrial lineages, all distinct from the populations from Peru (Fouquet et al. 2012). Therefore, we suspect that the population of the Mitaraka massif may not correspond to the nominal species. HABITAT IN MITARAKA. — This species was found conspicuously calling throughout the study area. MATERIAL EXAMINED. — La Planète Revisitée Guyane 2015, MNHN-PNI, APA973-1: AF2781; AF2819 (♀)., Published as part of Fouquet, Antoine, Vidal, Nicolas & Dewynter, Maël, 2019, The Amphibians of the Mitaraka massif, French Guiana, pp. 359-374 in Zoosystema 41 (19) on page 367, DOI: 10.5252/zoosystema2019v41a19, http://zenodo.org/record/3724809, {"references":["AMEZQUITA A., LIMA A. P., JEHLE R., CASTELLANOS L., RAMOS O., CRAWFORD A. J., GASSER H. & HODL W. 2009. - Calls, colours, shape, and genes: a multi-trait approach to the study of geographic variation in the Amazonian frog Allobates femoralis. Biological Journal of the Linnean Society 98: 826 - 838. https: // doi. org / 10.1111 / j. 1095 - 8312.2009.01324. x","FOUQUET A., NOONAN B. P., RODRIGUES M. T., PECH N., GILLES A. & GEMMELL N. J. 2012. - Multiple quaternary refugia in the eastern Guiana Shield revealed by comparative phylogeography of 12 frog species. Systematic Biology 61: 461 - 489. https: // doi. org / 10.1093 / sysbio / syr 130"]}

Skin swabbing, a minimally invasive DNA sampling method recently proposed for adult amphibians, was tested on the dendrobatid frog Allobates femoralis. I compared DNA yield from skin swabs and toe clips by evaluating obtained DNA concentrations and purity of extracts, as well as amplification success using eleven polymorphic microsatellite loci. I also tested whether storing skin swabs for two months at −20°C affected the properties of the extract or microsatellite analysis. Results show that skin swabs of adult A. femoralis suffered from high contamination and yielded significantly lower DNA quality and quantity, resulting in insufficient genotyping success, than DNA obtained from toe clips. The relatively dry skin in dendrobatid frogs may have impeded the collection of sufficient viable cells, and the presence of skin alkaloids and microbiota in the frog mucus may lead to high contamination load of skin swabs.

Sound radiation patterns have ecological implications in the effective communication between conspecifics, like optimization of the sound propagation, increase the likelihood to reach mates and to mitigate effects of sound scattering by environmental factors like vegetation. The territorial frog Allobates femoralis advertises its territory against conspecific males and attract females with advertisement calls. Here we report the nearly omnidirectional sound-radiation pattern of the advertisement call of A. femoralis. This sound spreading pattern allows the males to attract mates and repel rivals in all directions. Furthermore, A. femoralis males direct the advertisement call to conspecific neighbours after phonotactic orientation.

The diet of anuran species is based on a large variety of prey items, which may be related to the availability of prey in the environment. In Amazonia, studies on the diet of anurans have occurred mainly in primary forests. Because forest fragmentation promotes changes in the environment, it is expected that the diet of anuran species will also be affected. Here we describe the diet composition of anurans captured in a forest remnant at Fazenda Amoty, municipality of Plácido de Castro, state of Acre, Brazil. Stomach contents of 34 specimens of Allobates femoralis (Aromobatidae), Adenomera hylaedactyla, Engystomops freibergi (Leptodactylidae), Rhinella sp. (Bufonidae), and Elachistocleis muiraquitan (Microhylidae) had 877 prey items belonging to 19 prey categories. The diet of most species were arthropods. Myrmicinae ants (Hymenoptera, Formicidae) was the most abundant and frequent item in A. hylaedactyla, Rhinella sp. and A. femoralis stomachs. Termitidae (Isoptera) was the second most abundant taxon in Rhinella sp. and A. hylaedactyla, and the only taxon found eaten by E. freibergi and E. muiraquitan. Most studied species showed generalist diet, which is the habit for most anuran species. Contrarily, E. freibergi and E. muiraquitan are likely specialized in Isoptera. Made available in DSpace on 2019-10-02T00:41:12Z (GMT). No. of bitstreams: 1 26864.pdf: 763642 bytes, checksum: d098cf8266b3f4344adb0dadbe084387 (MD5) Previous issue date: 2019

Está bem estabelecido que a ocorrência das espécies depende das suas necessidades biológicas em determinados ambientes, e que as espécies estão distribuídas em manchas de habitats favoráveis que são separadas umas das outras por habitats inadequados. No entanto, determinar como a heterogeneidade do habitat interage com a distribuição e a densidade das espécies em várias escalas geográficas e como os processos históricos e atuais do ambiente influenciam o fluxo gênico ao longo da paisagem continua sendo um dos maiores desafios da ecologia e biologia evolutiva. Esse tipo de abordagem ainda é raro na Amazônia, especialmente quando se trata de anuros. O objetivo geral desta tese foi investigar o papel de gradientes ambientais na distribuição, abundância, variabilidade genética e fluxo gênico de Allobates femoralis ao longo de 880 km de paisagens heterogêneas que ocorrem no interflúvio entre os rios Purus e Madeira (IPM). No primeiro capítulo, testamos se as características do solo e da floresta estão associadas com a distribuição e abundância relativa de A. femoralis através do IPM. Nós mostramos que A. femoralis é mais abundante em florestas abertas e ausente ou raro em florestas densas e positivamente associado com solos ricos em argila. Nossos dados sugerem que a distribuição e abundância relativa dessa espécie é moldada por gradientes ecológicos graduais. No segundo capítulo, aplicamos uma abordagem de modelagem multinível baseada em dados genômicos e teoria dos circuitos para testar se a distância geográfica e o gradiente ambiental ao longo da paisagem heterogênea do IPM influenciam a variabilidade genética e o fluxo gênico de A. femoralis. Nós mostramos que os padrões espaciais de variabilidade genética e o fluxo gênico em A. femoralis são influenciados tanto pela distância geográfica quanto pelos gradientes ambientais, suportando assim a hipótese dos gradientes para diversificação. Nós também identificamos quatro grupos genéticos que foram associados com variações fenotípicas (cor da mancha femoral), forte divergência na parte nordeste do IPM que está relacionada a processos históricos e com a presença de diferentes tipos de floresta. Sugerimos que investigando o papel da heterogeneidade ambiental em outras espécies co-distribuídas irá fornecer dados que podem ser usados para melhor entender o papel de gradientes ambientais na diversificação parapátrica de espécies na Amazônia. It is well established that the occurrence of species depends on their biological needs in given environments, and that species are distributed to favorable habitat patches which are separated from each other by unsuitable habitats. However, determining how habitat heterogeneity interacts with the distribution and density of species at various geographic scales and how historical processes and the contemporary environment has influenced gene flow across landscapes remains one of the major challenges in ecology and evolutionary biology. This type of approach is still rare in Amazonia, especially when it comes to anurans. The main goals of this thesis were to investigate the role of environmental gradients on the distribution, abundance, genetic variability and gene flow of Allobates femoralis along 880 km of heterogeneous landscape in the interfluve between the Purus and Madeira rivers (PMI). In the first chapter, we tested whether soil and forest characteristics are associated with the distribution and relative abundance of A. femoralis along PMI. We show that A. femoralis is more abundant in open forests and absent or rare in dense forests and positively associated with clay-rich soils. Our findings suggest that the distribution and relative abundance of this species is shaped by gradual ecological clines. In the second chapter, we apply a multilevel modeling approach based on genomic data and circuit theory to test whether geographic distance and environmental gradients across the heterogeneous landscape of PMI influences the genetic variability and gene flow of A. femoralis. We show that spatial patterns of genetic variability and gene flow in A. femoralis are influenced by both geographic distance and environmental gradients, thus supporting the gradient hypothesis for diversification. We also identified four genetic clusters which partly paralleled phenotypic variation (femoral spot colour), strong divergence in the northeastern part of the PMI that is likely due to historical processes, and with the presence of different forest types. We suggest that investigating the role of environmental heterogeneity in other codistributed species will provide data that can be used to better understand the role of environmental gradients in the parapatric diversification of species in the Amazon.

The distribution of biodiversity within the Amazon basin is often structured by sharp environmental boundaries, such as large rivers. The Amazon region is also characterized by subtle environmental clines, but how they might affect the distributions and abundance of organisms has so far received less attention. Here, we test whether soil and forest characteristics are associated with the occurrence and relative abundance of the forest-floor dwelling Aromobatid frog,Allobates femoralis. We applied a structured sampling regime along an 880 km long transect through forest of different density. High detection probabilities were estimated forA. femoralisin each of the sampling modules. Using generalized linear mixed-effects models and simple linear regressions that take detectability into account, we show thatA. femoralisis more abundant in open forests than in dense forests. The presence and relative abundance ofA. femoralisis also positively associated with clay-rich soils, which are poorly drained and therefore likely support the standing water bodies required for reproduction. Taken together, we demonstrate that relatively easy-to-measure environmental features can explain the distribution and abundance of a widespread species at different spatial scales. Such proxies are of clear value to ecologists and conservation managers working in large inaccessible areas such as the Amazon basin.

The brilliant-thighed frog [Allobates femoralis (Boulenger, 1884)] is distributed across the Amazon basin and aggregates several allopatric evolutionary lineages, some of which present variation in their advertisement calls. In 2009, an unregistered call phenotype was discovered in the region of Altamira and Vitória do Xingu, State of Pará, Brazil, where males emit advertisement calls formed by six notes, differing from the typical four-note calls described for other A. femoralis populations. In this study, we describe in detail these untypical calls. Additionally, we test whether the aggressive responses of males of a 4-note reference population (Reserva Ducke - RFAD, in Manaus, States of Amazonas) is differential towards the 6-note calls of males recorded in Altamira (Pará State), and towards 4-note calls recorded in one location at the Tapajós-Xingu interfluve (Belterra, Pará State), and in RFAD. Playback experiments were conducted between 2011-2012, and used standardized stimuli produced from natural call recordings. A total of 30 independent experiments were conducted, 10 for each stimuli class. We measured the phonotaxis of focal males in relation to the loudspeaker, considering the time to orientation and the time to approach the loudspeaker. We found that not all A. femoralis males at RFAD promptly recognize calls from males recorded in Altamira. However, when considering only males who approached the loudspeaker, differences in aggressive reactions were not seen between stimuli classes. Our findings show that the ability to recognize calls from Altamira as belonging to co-specific males is not universal among males at RFAD. The new A. femoralis phenotype occurs in areas potentially impacted by the Belo Monte hydroelectric complex and complementary studies indicate that no gene flow exists between this group and A. femoralis from adjacent regions. Hence, developments in Altamira may put this incipient speciation process at risk. © 2017, Fundacao Zoobotanica do Rio Grande do Sul. All rights reserved.

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 frogAllobates femoralisduring 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 inA. 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.

Life history trade-offs in reproductive strategy are often invoked as ecological agents of evolutionary change, despite a limited amount of experimental data from the field. The larval deposition strategy of Allobates femoralis was tested in Southeastern Peru using a blocked, fully crossed experimental design. Arrays of four pools were used to test the effects of pool size and the presence of a predatory insect (Belostomatid) on the deposition behavior of A. femoralis. Further experiments investigated the colonization of insect predators into potential larval habitats and interactions between predatory insects. Results suggest that pool size, the presence of predatory aquatic insects, and interactions between predators, influence larval deposition in A. femoralis. Similar ecological interactions may have driven toxic dendrobatids to the use of arboreal phytotelmata and associated derived reproductive strategies.

This Special Issue demonstrates the breadth of evolutionary ecology research occurring on Neotropical poison frogs (Dendrobatidae). It also draws attention to the incredible diversity of the poison frogs themselves (phenotypic, behavioral and taxonomic diversity) and this group's potential for research programs focusing on speciation, the evolution of toxicity, color pattern diversity, Mullerian and Batesian mimicry, sexual selection, mating systems and parental care. This Special Issue focused on two key research foci in the field of evolutionary ecology: (1) Understanding the interplay between ecology and the evolution of parental care and (2) Elucidating the ecological factors contributing to the evolution of toxicity, aposematism and color pattern diversity. In this paper, I summarize the major findings of studies presented in this Special Issue. Understanding the interplay between ecology and the evolution of parental care Parent poison frogs transport and subsequently deposit their tadpoles in pools of water. The evolutionary transition from terrestrial to smaller arboreal phytotelmata for tadpole deposition is thought to be driven by a reduction in competition and predation associated with smaller tadpole nurseries. This transition is considered a key evolutionary innovation, allowing access to relatively unexploited resources and facilitating the evolution of many novel breeding strategies. To date, there are only a few empirical examples in dendrobatids to support this hypothesis (Weygoldt 1980; Caldwell 1997; Brown et al. 2010). Field experimentation by McKeon and Summers (2013) present a more complete picture of the interactions between the natural history of Allobates femoralis and the tadpole predators present. Their results suggest that pool size, the presence of predatory insects and inter- actions between predators (and indirect effects on tadpoles) influence larval deposition in A. femoralis. Previous research on Ranitomeya species, a genus distantly related to Allobates, has demonstrated that adults also assess multiple aspects of reproductive resources to

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.

Field observations and mark–recapture sampling carried out in the Reserva Ducke in Central Amazonia provided information on the occurrence of reproductive events of the Brilliant-Thighed Frog, Allobates femoralis, in the context of seasonal rainfall. In addition, we report on the daily pattern of calling activity and the use of space by marked individuals. Rainfall was a strong determinant of the calling and breeding activities at a seasonal scale. The phenology of A. femoralis was affected by interannual differences in both the length and severity of the dry season. This species showed a consistent diel pattern throughout the year, with calling activity peaking between 1500 and 1600 h. At the seasonal scale, calling activity was higher during the wet months and was correlated positively with monthly rainfall. Although recruitment is concentrated in the late wet season, our observations of juveniles in the smallest size classes throughout the year indicated that reproduction occurs sporadically e...

In species-rich assemblages of acoustically communicating animals, heterospecific sounds may constrain not only the evolution of signal traits but also the much less-studied signal-processing mechanisms that define the recognition space of a signal. To test the hypothesis that the recognition space is optimally designed, i.e., that it is narrower toward the species that represent the higher potential for acoustic interference, we studied an acoustic assemblage of 10 diurnally active frog species. We characterized their calls, estimated pairwise correlations in calling activity, and, to model the recognition spaces of five species, conducted playback experiments with 577 synthetic signals on 531 males. Acoustic co-occurrence was not related to multivariate distance in call parameters, suggesting a minor role for spectral or temporal segregation among species uttering similar calls. In most cases, the recognition space overlapped but was greater than the signal space, indicating that signal-processing traits do not act as strictly matched filters against sounds other than homospecific calls. Indeed, the range of the recognition space was strongly predicted by the acoustic distance to neighboring species in the signal space. Thus, our data provide compelling evidence of a role of heterospecific calls in evolutionarily shaping the frogs' recognition space within a complex acoustic assemblage without obvious concomitant effects on the signal.

The call of the pan-Amazonian frog Allobates femoralis shows wide geographical variation, and males show a stereotyped and conspicuous phonotactic response to playback of conspecific calls. We evaluated the capacity of males of A. femoralis and a closely related species A. hodli to respond aggressively to natural conspecific and heterospecific calls varying in number of notes, by means of field playback experiments performed at two sites in the Brazilian Amazon. The first site, Cachoeira do Jirau (Porto Velho, Rondonia), is a parapatric contact zone between A. femoralis that use 4-note calls, and A. hodli with 2-note calls, where we performed cross-playbacks in both focal populations. The second site, the Reserva Florestal Adolpho Ducke (Manaus, Amazonas), contained only A. femoralis with 4-note calls. There, we broadcast natural stimuli of 2-note A. hodli, 3-note and 4-note A. femoralis, and 6-note A. myersi. We found that the phonotactic behaviour of A. femoralis and A. hodli males did not differ toward conspecific and heterospecific stimuli, even in parapatry. Our results indicated that the evolutionary rates of call design and call perception are different, because the geographical variation in calls was not accompanied by variation in the males' aggressive behaviour.

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.

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 3 months 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 accuracy 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 intervals, 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 interbout 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'.

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.

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.

One or both sexes exhibit territorial behavior in all dendrobatids that have been studied. Two types of territoriality are identified. In some Colosthethus species only females or both sexes defend small nonreproductive territories that offer access to water, food, and shelter. In other species, only males defend large reproductive territories against conspecific calling males, suggesting that females are the limited resource. However, in no case has the defended resource been unambiguously identified. I hypothesize that, in at least some species, males compete for calling sites in areas with high female density and with favorable sound transmission features. I found little support for the hypothesis that dendrobatids exhibit resource defense polygyny. More research is necessary to understand the function of territoriality and to identify limiting resources in poison frogs.

The phenology of calling activity and reproduction of a neotropical anuran community in French Guiana was studied during one rainy season. We investigated the correlation between calling activity, rainfall, temperature and water level in two ponds and recorded the occurrence of tadpoles of pond-breeding species. The study site contained 31 calling frog species, which were divided into groups according to reproductive mode. Increased rainfall was associated with increased reproductive activity in all groups, but temporal patterns in calling activity varied significantly between groups. Species with aquatic oviposition exhibited sporadic acoustic activity, aggregating into explosive breeding events following heavy rainfall. Species laying eggs in foam nests had the peak of calling activity at the start of the rainy season. Taxa with embryonic development on vegetation called mainly from middle to late wet season, being the only group which showed a significant correlation of calling with increasing water level. Dendrobatids with terrestrial oviposition and subsequent parental tadpole transportation were continuously active. Species with direct development or with non-feeding larvae were mainly active at the beginning of the rainy season. It is concluded that phenologies of calling activity in South American tropical anuran species are strongly influenced by abiotic factors like rainfall and availability of breeding sites. The temporal limitation of the rainy season forces species to adjust calling and reproductive activity according to their reproductive modes.

The distribution of many vertebrate species in the Amazon basin is delimited by large rivers, which are frequently regarded as geographic barriers related with speciation and are therefore of high conservation value. Rapid development in the region includes plans to dam one of its thirteen major rivers, the Xingu. Environmental impact assessment is required for large scale development within the Brazilian portion of the Amazon Basin. However, impacts on biodiversity are only considered at the species level, and taxonomic work is far from described for many groups. In particular, anuran diversity is underestimated, in part owing to the scale of the region and, for some taxa, by morphological conservatism. Here we describe genetic and phenotypic variation in the brilliant-thighed frog, Allobates femoralis. We show that a unique genetic lineage, with a vocal repertoire distinct from that described for the species throughout its remaining geographic range, is located within the region to be directly and indirectly impacted by damming the Xingu River. Further, genetic variation within the A. femoralis group is largely structured in accordance to river systems, despite morphological conservatism. Our data add support for conservation policy to be amended to include intraspecific measures of diversity in order to more effectively conserve current biodiversity and evolutionary processes. © Pedro Ivo Simões, Adam Stow, Walter Hödl, Adolfo Amézquita, Izeni P. Farias and Albertina P. Lima.

Introduction 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. Results 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. Conclusions 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.

The adaptive significance of sequential polyandry is a challenging question in evolutionary and behavioral biology. Costs\ud and benefits of different mating patterns are shaped by the spatial distribution of individuals and by genetic parameters\ud such as the pairwise relatedness between potential mating partners. Thus, females should become less choosy as costs of\ud mating and searching for mates increase. We used parentage assignments to investigate spatial and genetic patterns of\ud mating across a natural population of the Neotropical frog Allobates femoralis, a species characterized by male territoriality\ud and care and female iteroparity. There was no correlation between genetic and spatial distances between adult individuals\ud across the population. In 72% of cases, females mated with males available within a radius of 20 m. Mean pairwise\ud relatedness coefficients of successful reproducers did not differ from random mating but had a lower variance than\ud expected by chance, suggesting maximal reproductive output at intermediate genetic divergence. We also found evidence\ud for selection in favor of more heterozygous individuals between the embryo and adult stage. The level of sequential\ud polyandry significantly increased with the number of spatially available males. Females that had more candidate males also\ud produced more adult progeny. We hypothesize that the benefits associated with female multiple mating outweigh the\ud costs of in- and outbreeding depression, and consequently precluded the evolution of ‘choosy’ mate selection in this\ud species.

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.

Linking specific ecological factors to the evolution of parental care pattern and mating system is a difficult task of key importance. We provide evidence from comparative analyses that an ecological factor (breeding pool size) is associated with the evolution of parental care across all frogs. We further show that the most intensive form of parental care (trophic egg feeding) evolved in con- cert with the use of small pools for tadpole deposition and that egg feeding was associated with the evolution of biparental care. Previous research on two Peruvian poison frogs (Ranitomeya imitator and Ranitomeya variabilis) revealed similar life histories, with the excep- tion of breeding pool size. This key ecological difference led to di- vergence in parental care patterns and mating systems. We present ecological field experiments that demonstrate that biparental care is essential to tadpole survival in small (but not large) pools. Field observations demonstrate social monogamy in R. imitator, the species that uses small pools. Molecular analyses demonstrate genetic mo- nogamy in R. imitator, the first example of genetic monogamy in an amphibian. In total, this evidence constitutes the most complete documentation to date that a single ecological factor drove the evo- lution of biparental care and genetic and social monogamy in an animal.