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Wetland hydroperiod affects the ecology and evolution of numerous freshwater organisms. Pond-breeding amphibians are particularly affected by hydroperiod, with their life histories and distributional patterns often resulting from how long ponds remain inundated. Substantial variability exists among species in their responsiveness to fluctuations in hydroperiod, making taxon-specific investigations needed to understand its general impacts. We tested whether two fall-breeding salamanders, Ambystoma annulatum and A. opacum, each of which have long (> 6 month) larval period durations, respond to variation in hydroperiod length. We manipulated hydroperiod in outdoor experimental mesocosms under three scenarios (short hydroperiod, medium hydroperiod, and constant water levels), focusing specifically on how hydroperiod affected their life history traits (survival, size, and time to metamorphosis). We found that in the shortened hydroperiod treatments, few individuals of either species completed metamorphosis and would have died, whereas nearly all surviving individuals underwent metamorphosis under longer hydroperiod treatments. After correcting for differences in survival, body size at metamorphosis was greater in constant hydroperiod treatments for only A. annulatum. Larval periods were on average longer in constant hydroperiods for both species. The relationship between size and time to metamorphosis was positive for both A. annulatum and A. opacum, with limited differences between hydroperiod treatments in this relationship for either species. Overall, these results indicate these fall-breeding species are indeed affected by hydroperiod variation, but in different ways, depending on the life history response. These diverse responses highlight the complexities of building generalized responses of amphibians to a shared stressor like hydroperiod variation, as taxon- and trait-specific responses appear to be common. Future work should consider other aspects of hydroperiod as a structuring abiotic force (e.g., onset of drying), or the life history traits of amphibians (e.g., their breeding phenology), to better understand the ecology and evolution of pond-breeding amphibians, as well as provide insights into management actions for their conservation.
A taxonomic revision of the genus Centrogenys (family: Centrogenyidae), having previously been regarded as monotypic (also monotypic family) represented by Centrogenys vaigiensis, resulted in the recognition of three species, including two new species from Australia, Centrogenys algrahami, new species, and Centrogenys pogonoskii, new species. The two other nominal species of the genus, Centropristes scorpenoides and Sebastes stoliczkae, were regarded as junior synonyms of C. vaigiensis. Centrogenys vaigiensis is readily distinguished from the two new species by lacking scale patches on the membranes between dorsal-fin spines (a small patch of scales present on each interspinous membrane of the third to last dorsal-fin spines in the two new species). Centrogenys algrahami, new species, is characterized by having fewer body scales, including 31–36 pored lateral-line scales (vs. 37–44 in C. vaigiensis and 39–46 in C. pogonoskii, new species) and 31–36 scale rows in longitudinal series (vs. 36–43 and 39–47), and a slightly greater number of pectoral-fin rays 14–16 (modally 15; vs. 12–15 [modally 14] in C. vaigiensis and C. pogonoskii, new species). Moreover, C. pogonoskii, new species, is distinguished from the two congeners by the presence of squamation on the lateral side of the snout (in specimens >34 mm SL), whereas it is naked in the congeners. The status of the three species resulting from the morphological analysis was also strongly supported by molecular evidence of a partial sequence of the COI gene. Centrogenys vaigiensis is widely distributed in the Indo-West Pacific, ranging from Mauritius east to Indonesia and north to southern Japan. In contrast, Centrogenys algrahami, new species, and Centrogenys pogonoskii, new species, are restricted to Australia.
The bowfins, Amia, have been regarded as regarded as promiscuous or polygynous spawners, although this has not been directly observed. Species of Amia spawn largely at night in male-constructed and male-guarded nests, making it difficult to view spawning behavior. Furthermore, in many species, field observations of spawning behavior do not always match genetic observations. To investigate the mating system of Amia, we collected fin tissue from guarding males and a sample of associated eggs or fry from 15 broods to assess the number of parents involved in each brood. Using these tissues, we genotyped individuals at 11 microsatellite DNA loci. The genotype of the male was known; we inferred the genotype of the primary female by subtraction, using the most abundant fry genotypes and the known male genotype. We inferred polygamy (presence of multiple fathers or multiple mothers) in cases where there was more than a single fry at a single locus for which the genotype could not be explained by primary parental genotypes. Among sampled broods, seven contained offspring of a single male–female pair. Fry from eight broods show evidence of polygamy: in one brood, there was evidence of an extra-pair male; in five broods, there was evidence of at least one additional female, and in two of these five broods, there was also involvement by at least one additional male; in two broods, it could not be determined whether the additional parent was male or female. Thus, nearly half of our sampled broods were both behaviorally and genetically monogamous, while other broods were genetically polygamous. It has been suggested previously that female bowfin may spawn with more than one male, but there are no behavioral observations to support this claim and our genetic data cannot discern whether females are spawning in more than one nest. We conclude that Amia is behaviorally monogamous and weakly genetically polygynous. With respect to the evolution of mating systems of fishes, it is interesting that Amia, representing a member of the Holostei or the sister group to teleosts, is behaviorally monogamous, albeit with opportunistic participation in spawning by either extra males or extra females or both. A review of the literature on spawning behavior of non-teleostean ray-finned fishes suggests that additional behavioral and genetic studies of these fascinating taxa are warranted.
Resource allocation and hormone provisioning during vitellogenesis has been documented for many oviparous reptiles, while viviparous species remain relatively understudied in the context of yolk composition. Squamates that have evolved viviparity have retained varying degrees of embryonic nourishment via the yolk (lecithotrophy). Very little is known about the timing of embryonic hormone production, and the degree of maternal hormone provisioning in viviparous reptiles. Viviparous species may, in principle, receive hormone exposure through some or all of three routes, viz., maternal provisioning in the yolk, transfer from the maternal circulation, and/or hormone production by the developing embryonic endocrine tissues. In toad-eating snakes, adrenal hormones may provide protection from toad toxins, supplementing genetic resistance. Additionally, one species of oviparous snake has been shown to provision its embryos with defensive toxins from toads. We hypothesized that embryonic hormone levels would increase during development and that yolk hormone levels would correspondingly decrease. We also predicted that the embryos from females administered toad toxin would have higher levels of corticosterone (CORT) in response to exposure to a toad toxin. We measured levels of CORT in the embryos and corresponding yolks of a viviparous and genetically toxin-resistant natricine, the Western Terrestrial Garter Snake (Thamnophis elegans), beginning at Zehr Stage 26. We found that embryos and their corresponding yolks had relatively higher levels of CORT in later stages. There were no measurable differences in CORT between embryos of the same stage obtained from dams treated with marinobufagenin (MBG) or no treatment. Given that yolk and embryonic CORT increase throughout the course of development, a trade-off between early maternal provisioning and the onset of adrenal function is not apparent. However, increase in adrenal production of CORT over the course of development remains relevant to both stress physiology and physiological toxin resistance.
Examination of the original description of Thrissina malabarica (Bloch, 1795), a name previously applied to an Indian Ocean species with a distinctly deep body, revealed that the former nominal species was actually a senior synonym of Thrissina hamiltonii (Gray, 1835), a slender-bodied Indo-West Pacific species. The applicable name for the species previously treated as T. malabarica is Thrissina cuvierii (Swainson, 1839). To stabilize the taxonomic status of these three nominal species, a neotype for T. cuvierii is designated. In addition, Thrissina aurora, new species, is described from a specimen collected from the Andaman Sea near Phuket, Thailand. Although both the new species and T. cuvierii share a deep body, the former is distinguished by lower counts of gill rakers and anal-fin rays than the latter. The mitochondrial cytochrome oxidase I (COI) haplotype network of 11 specimens of T. cuvierii and three specimens (including the holotype) of T. aurora, new species, revealed 22 nucleotide differences between the two species, corresponding to 3.4% mean uncorrected genetic distance.
To evaluate the utility of a deep-learning approach for monitoring amphibian reproduction, we examined the classification accuracy of a trained model and tested correlations between calling intensity and frog abundance. Field recording and count surveys were conducted at two sites in Kyoto City, Japan. A convolutional neural network (CNN) model was trained to classify the calls of five anuran species. The model achieved 91–100% precision and 75–98% recall per species, with relatively lower performance on less abundant species. Computational experiments investigating the effects of the number and seasonality of the training samples showed that models trained on larger datasets from broader recording seasons performed better. Calling activity was high when males were abundant (Pearson's r = 0.45–0.66), although correlations between the calling activity and the number of pairs in amplexus were generally weaker. Our results suggest that deep learning is an effective tool for reconstructing the reproductive phenology of male anurans from field recordings. However, caution is required when applying to rare species and when inferring female reproductive activity.
Since the early 1990s, > 3,000 ha of wetlands (and adjacent prairie) have been restored on the row-crop agricultural landscape of Winnebago County, Iowa, U.S.A. From 2014–2016, we surveyed 45 wetlands among 19 easements for occupancy by Eastern Tiger Salamanders (Ambystoma tigrinum tigrinum) and used radio-telemetry to measure their patterns of movement and habitat use. Rates of occupancy increased with wetland age, from < 25% for wetlands 1–2 years old to ∼75% for wetlands > 11 years old. A two-year survey (2014 and 2015) of ten wetlands restored in 2013 showed that nine were occupied after two years; we did not find a relationship between distance to the nearest salamander population and occupancy of newly restored wetlands by salamanders. We tracked 30 salamanders after they left their breeding wetlands for an average of 69±37 d (range = 14–109 d) and relocated them a total of 393 times. Typically, once a salamander left its breeding wetland, it traveled 50–350 m over several days, found a suitable burrow, then remained for much of the rest of the season. Mean daily distances traveled by salamanders were 7.9±5.6 m (range = 0–135 m); the range of maximum straight-line distances moved was 26–659 m; only one individual salamander traveled in a statistically linear path, relative to a random walk. While ∼90% of the landscape was composed of row-crop fields, salamanders used protective grassy habitats (e.g., restored prairie, road ditches) on ∼88% of our observations. Only three salamanders used row-crop fields, and two of them were killed by heavy equipment. Regardless of the terrestrial habitat types used by salamanders, we found them underground on 336 (84.8%) of our observations.
Biotic indices (bioindicators) can be individual species, species groups, or communities of species used to assess habitat quality. But, to be used effectively, managers require basic information on species used as indicators, including species distribution, differentiation between similar species, and environmental conditions associated with species presence. We addressed these problems concurrently in two related species, the Mottled Sculpin (Cottus bairdii) and the Slimy Sculpin (Cottus cognatus), as habitat quality indicators in the Manistee River in Michigan, USA. We determined the abundance and distribution of these species and related their presence to concurrent in-stream measurements of temperature, dissolved oxygen, pH, conductivity, turbidity, and stream quality score based on macroinvertebrate diversity. Cladistic analyses of CO1 supported recognition of Mottled Sculpin and Slimy Sculpin as distinct species and confirmed initial field identification to species using morphological characteristics. Both species were most abundant in headwater regions, decreased downstream, and were sympatric at 5 of 12 (42%) locations. Mottled Sculpin were associated with lower conductivity, pH, and stream quality scores. Slimy Sculpin were associated with higher levels of DO and lower levels of turbidity. As a management indicator species of the US Forest Service, Mottled Sculpin alone may be ineffective as a habitat quality indicator, but concurrent use of Mottled Sculpin and Slimy Sculpin as a related-species complex might allow sufficient coverage to permit assessment of stream quality if species-specific differences in environmental tolerances are precisely determined.
A time-calibrated phylogeny, based on nuclear ultraconserved elements and including representatives of all major alestid lineages, strongly supports two distantly related clades within the currently accepted concept of Brycinus. The first, which includes the type species of the genus, B. macrolepidotus (herein Brycinus), and a second, composed of taxa previously referred to as the B. nurse group (herein Brachyalestes), are both resolved as monophyletic. These results provide strong evidence for the restriction of the genus Brycinus to nine species, and for the revalidation of the genus Brachyalestes to accommodate 20 valid species. Within Brachyalestes, a new species from the Lulua River basin, initially misidentified as Brycinus kingsleyae, is described and resolved as sister to the widespread, central Congolese lowland species, Brachyalestes bimaculatus. Within Brachyalestes, a subclade mostly restricted to the Central Congo basin is estimated to have undergone diversification within the last 10 million years, suggesting that Late Neogene riverine reorganization likely influenced their allopatric speciation. The split of the new species, endemic to high elevation tributaries of the Lulua River, from its lowland sister species, Brachyalestes bimaculatus, suggests a Late Miocene/Early Pliocene colonization into the upland river ecosystems of the Katanga plateau in the southwestern Democratic Republic of Congo.
Photographic mark–recapture is a recently developed method that uses photographs of naturally occurring body patterns to identify individual animals. This method may be especially appropriate for amphibians because they are difficult to externally mark for individual recognition. However, the reliability of the method depends on whether or not the considered pattern differs consistently among individuals over time. We took pictures of the black and yellow thigh pattern of Cope's Gray Treefrogs (Hyla chrysoscelis) across two years to test whether this trait was consistent enough that individuals could be recognized from photographs, using automated photo recognition in Wild-ID software. We tested the performance of this program using sample sets of photos taken at three different timescales: photos from the same night, different nights within a year, and two different years. We also tested whether the likelihood of correct identifications decreased with increasing sample size. Overall, photographic mark–recapture produced a very high percentage of correct identifications across all timescales and sample sizes. Thus, we conclude that the use of this inexpensive and non-invasive technique on the thigh color pattern of H. chrysoscelis is a highly effective method for individual recognition.
El marcaje–recaptura fotográfico es un método de reciente desarrollo que emplea fotografías de patrones corporales distintivos que aparecen de forma natural para identificar a los animales individualmente. Este método puede ser particularmente apropiado en anfibios ya que son difíciles de marcar externamente para su reconocimiento individual. Sin embargo, la fiabilidad del método depende del potencial que tiene el patrón considerado para diferir de forma consistente entre individuos a lo largo del tiempo. Se tomaron fotografías del patrón negro-amarillo del muslo en la rana arbórea Hyla chrysoscelis a lo largo de dos años para testar si este rasgo era suficientemente consistente como para que los individuos fueran reconocidos a partir de fotografías empleando el programa automático de foto reconocimiento Wild-ID. Examinamos el rendimiento del programa usando series muestrales de fotografías tomadas a tres escalas temporales distintas: fotografías tomadas durante la misma noche, entre noches dentro del mismo año, y entre dos años. También se exploró si la probabilidad de identificaciones correctas se redujo al incrementar el tamaño muestral. En general, la captura–recaptura fotográfica produjo un alto porcentaje de identificaciones correctas en todas las escalas temporales y tamaños muestrales. Así, concluimos que el uso de esta técnica barata y no invasiva en el patrón de color del muslo de H. chrysoscelis es un método altamente efectivo para el reconocimiento individual.
Secondary sexual dimorphism is relatively common in the ghost knifefishes (Gymnotiformes: Apteronotidae), with males of several species growing greatly elongated snouts (e.g., Compsaraia samueli, Parapteronotus hasemani), while others develop enlarged, protruding teeth on either the lower jaw (Sternarchorhynchus spp.) or both jaws (Sternarchogiton nattereri). Of the four known species of Sternarchogiton, sexual dimorphism has so far only been reported in S. nattereri. Here we report that in an additional species, S. labiatus, mature males possess similar enlarged, external teeth on the dentary and premaxilla. We document this condition in three specimens collected during the high-water spawning season from the río Nanay near Iquitos, Peru. We analyze this morphology using high-resolution X-ray microcomputed tomography. Additionally, we use genetic sequence data to demonstrate that specimens bearing external teeth are genetically indistinguishable from those with the phenotype of S. labiatus. Finally, we review and summarize the current knowledge of sexual dimorphism within the Apteronotidae.
Abiotic filters like high gradients or hydraulic drops play an integral role in excluding species from interacting with some headwater communities. When humans manipulate the ecosystems to install small ponds in the headwaters of river networks, they allow stocked species of fishes to escape and bypass these filters creating novel communities already under stress from other environmental changes. We investigated a novel headwater community to assess if and how escaped Lepomis spp. compete with a native headwater fish, Chrosomus tennesseensis (Tennessee Dace). We designed an ex situ mesocosm study to test the effects of exploitative and interference competition by two species—L. macrochirus and L. cyanellus—on C. tennesseensis. We observed strong intraspecific competition that exceeded the effects of both Lepomis spp. on C. tennesseensis. Although one individual was always a clear winner in intraspecific interactions, morphology at the beginning of the experiment could not explain why one individual was more successful than another. We also observed marginally higher growth rate in C. tennesseensis when Lepomis spp. were caged rather than free-swimming indicating that introduced Lepomis spp. likely impact headwater fishes through exploitative and interference competition in addition to the potential of predation at large size differences. More research is needed to understand the breadth and magnitude of potential problems posed by the unintentional introduction of stocked fishes to low-order streams.
Urspelerpes brucei (Patch-nosed Salamander) is a miniaturized lungless salamander (family Plethodontidae) native to select headwater tributaries of the Tugaloo River along the border of Georgia and South Carolina. Due to the rarity and relatively recent discovery of this species, many aspects of its biology are unstudied. In particular, there has not yet been any description of its larval skeleton. We provide the first description of larval osteology for U. brucei, and we compared cleared and stained specimens of U. brucei close to the minimum size at metamorphosis to similarly sized specimens of Eurycea cirrigera (Southern Two-lined Salamander). Our results showed that the skull and long bones of U. brucei are more heavily ossified at smaller sizes than in E. cirrigera. In addition, U. brucei possesses more robust vomers and pterygoids, coronoids that are already incorporated into the dentary, and an ossified os thyroideum. These discrepancies in ossification suggest that the skeletons of U. brucei complete development at smaller sizes than E. cirrigera, a result likely tied to heterochronic accelerations of mineralization and sexual maturation in U. brucei. Taken together, these factors appear to help explain how U. brucei has developed and maintained its small body size.
Resource availability not only determines species assemblages but can also influence local density. The critical resource for a species or population is not always obvious. Among poison frogs (Dendrobatidae), whose populations are not limited by predation due to their toxicity, resource limitation may be key in determining density of a population. Strawberry Poison Frogs, Oophaga pumilio, are a small dendrobatid in Central America that exhibits parental care at specialized nest sites in rearing of offspring. Resources that may influence population density are varied, although nest sites with available food and ability to rear offspring are likely important factors. We sought to assess how population demographics changed with alterations to food and rearing sites in one population of O. pumilio on Isla Colon of Bocas del Toro, Panama. To test this hypothesis, we established 18 plots and made observations June–August 2009 and May–June 2010. We manipulated resources by the addition or removal of leaf litter and by providing artificial rearing sites. Artificial rearing sites were large diameter drinking straws folded in half to catch water, mimicking the water tanks found in bromeliads. Population density was not affected by manipulations of leaf litter, suggesting that food resources are not limiting to local density. However, artificial rearing sites were found to have a significant effect; on average, addition of artificial rearing sites resulted in doubling of the population. This study demonstrates that availability of offspring rearing sites is an important limiting resource for phytotelmata-breeding amphibians.
La disponibilidad de recursos no solo determina los conjuntos de especies, sino que también puede influir en el tamaño de la población. El recurso crítico para una especie o población no siempre es obvio. Entre las ranas venenosas (Dendrobatidae), cuyas poblaciones no están limitadas por la depredación debido a su toxicidad, la limitación de recursos puede ser clave para determinar el tamaño de la población. Las ranas venenosas de fresa, Oophaga pumilio, son un pequeño dendrobátido de América Central que exhibe cuidados parentales en nidos especializados en la crianza de crías. Los recursos que pueden influir en el tamaño de la población son variados, aunque los sitios de anidación con comida disponible y la capacidad de criar crías probablemente sean factores importantes. Buscamos evaluar cómo cambió la demografía de la población con alteraciones en la alimentación y los sitios de crianza en una población de O. pumilio en Isla Colón de Bocas del Toro, Panamá. Para probar esta hipótesis, establecimos 18 parcelas e hicimos observaciones de junio a agosto de 2009 y de mayo a junio de 2010. Manipulamos los recursos mediante la adición o eliminación de hojarasca y proporcionando sitios de cultivo artificiales. Los sitios de crianza artificial eran pajillas para beber de gran diámetro dobladas por la mitad para atrapar agua, imitando los tanques de agua que se encuentran en las bromelias. La densidad de población no se vio afectada por la manipulación de la hojarasca, lo que sugiere que los recursos alimentarios no se limitan al tamaño de la población. Sin embargo, se encontró que los sitios de crianza artificial tienen un efecto significativo; en promedio, la adición de sitios de crianza artificial resultó en la duplicación de la población. Este estudio demuestra que la disponibilidad de sitios de cría de crías es un recurso limitante importante para los anfibios reproductores de phytotelmata.
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