Janalee P. Caldwell

Declining amphibian populations : the problem of separating human impacts from natural fluctuations

Reports of declining amphibian populations in many parts of the world are numerous, but supporting long-term census data are generally unavailable. Census data from 1979 to 1990 for three salamander species and one frog species at a breeding pond in South Carolina showed fluctuations of substantial magnitude in both the size of breeding populations and in recruitment of juveniles. Breeding population sizes exhibited no overall trend in three species and increased in the fourth. Recent droughts account satisfactorily for an increase in recruitment failures. These data illustrate that to distinguish between natural population fluctuations and declines with anthropogenic causes may require long-term studies.

PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE)

Abstract The known diversity of dart-poison frog species has grown from 70 in the 1960s to 247 at present, with no sign that the discovery of new species will wane in the foreseeable future. Although this growth in knowledge of the diversity of this group has been accompanied by detailed investigations of many aspects of the biology of dendrobatids, their phylogenetic relationships remain poorly understood. This study was designed to test hypotheses of dendrobatid diversification by combining new and prior genotypic and phenotypic evidence in a total evidence analysis. DNA sequences were sampled for five mitochondrial and six nuclear loci (approximately 6,100 base pairs [bp]; x¯ = 3,740 bp per terminal; total dataset composed of approximately 1.55 million bp), and 174 phenotypic characters were scored from adult and larval morphology, alkaloid profiles, and behavior. These data were combined with relevant published DNA sequences. Ingroup sampling targeted several previously unsampled species, including Aromobates nocturnus, which was hypothesized previously to be the sister of all other dendrobatids. Undescribed and problematic species were sampled from multiple localities when possible. The final dataset consisted of 414 terminals: 367 ingroup terminals of 156 species and 47 outgroup terminals of 46 species. Direct optimization parsimony analysis of the equally weighted evidence resulted in 25,872 optimal trees. Forty nodes collapse in the strict consensus, with all conflict restricted to conspecific terminals. Dendrobatids were recovered as monophyletic, and their sister group consisted of Crossodactylus, Hylodes, and Megaelosia, recognized herein as Hylodidae. Among outgroup taxa, Centrolenidae was found to be the sister group of all athesphatanurans except Hylidae, Leptodactyidae was polyphyletic, Thoropa was nested within Cycloramphidae, and Ceratophryinae was paraphyletic with respect to Telmatobiinae. Among dendrobatids, the monophyly and content of Mannophryne and Phyllobates were corroborated. Aromobates nocturnus and Colostethus saltuensis were found to be nested within Nephelobates, and Minyobates was paraphyletic and nested within Dendrobates. Colostethus was shown to be rampantly nonmonophyletic, with most species falling into two unrelated cis- and trans-Andean clades. A morphologically and behaviorally diverse clade of median lingual process-possessing species was discovered. In light of these findings and the growth in knowledge of the diversity of this large clade over the past 40 years, we propose a new, monophyletic taxonomy for dendrobatids, recognizing the inclusive clade as a superfamily (Dendrobatoidea) composed of two families (one of which is new), six subfamilies (three new), and 16 genera (four new). Although poisonous frogs did not form a monophyletic group, the three poisonous lineages are all confined to the revised family Dendrobatidae, in keeping with the traditional application of this name. We also propose changes to achieve a monophyletic higher-level taxonomy for the athesphatanuran outgroup taxa. Analysis of character evolution revealed multiple origins of phytotelm-breeding, parental provisioning of nutritive oocytes for larval consumption (larval oophagy), and endotrophy. Available evidence indicates that transport of tadpoles on the dorsum of parent nurse frogs—a dendrobatid synapomorphy—is carried out primitively by male nurse frogs, with three independent origins of female transport and five independent origins of biparental transport. Reproductive amplexus is optimally explained as having been lost in the most recent common ancestor of Dendrobatoidea, with cephalic amplexus arising independently three times.

Amazonian Amphibian Diversity Is Primarily Derived from Late Miocene Andean Lineages

The Neotropics contains half of remaining rainforests and Earths largest reservoir of amphibian biodiversity. However, determinants of Neotropical biodiversity (i.e., vicariance, dispersals, extinctions, and radiations) earlier than the Quaternary are largely unstudied. Using a novel method of ancestral area reconstruction and relaxed Bayesian clock analyses, we reconstructed the biogeography of the poison frog clade (Dendrobatidae). We rejected an Amazonian center-of-origin in favor of a complex connectivity model expanding over the Neotropics. We inferred 14 dispersals into and 18 out of Amazonia to adjacent regions; the Andes were the major source of dispersals into Amazonia. We found three episodes of lineage dispersal with two interleaved periods of vicariant events between South and Central America. During the late Miocene, Amazonian, and Central American-Chocoan lineages significantly increased their diversity compared to the Andean and Guianan-Venezuelan-Brazilian Shield counterparts. Significant percentage of dendrobatid diversity in Amazonia and Chocó resulted from repeated immigrations, with radiations at <10.0 million years ago (MYA), rather than in situ diversification. In contrast, the Andes, Venezuelan Highlands, and Guiana Shield have undergone extended in situ diversification at near constant rate since the Oligocene. The effects of Miocene paleogeographic events on Neotropical diversification dynamics provided the framework under which Quaternary patterns of endemism evolved.

Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia

A population of the tropical lizard Tropidurus hispidus , isolated on a granitic rock outcrop in tropical forest of northern Brazil, was studied during the 1993 wet season. Four types of observational studies revealed that lizards are active throughout most of the day. During 10-minute intervals, individual lizards moved five times for an average of 240 cm and tongue-flicked once. Habitat temperatures vary considerably during the day, with rock and air temperatures in sun exceeding body temperatures of lizards during much of the activity period. During most of the day, lizards thermoregulate by moving among shady, filtered sun, and sunny microhabitats maintaining body temperatures near 35°C. Temperatures of lizards active during cloudy periods were significantly lower than temperatures of lizards during sunny periods, indicating that clouds decrease the ability of lizards to effectively thermoregulate. Most feeding occurs in the afternoon at edges of rock outcrops with ants, insect larvae, termites and beetles dominating the diet. Comparisons with a near-by savanna population revealed differences in body size (males only), activity period (longer on rocks), body temperatures (higher on rocks), number of prey categories consumed (lower on rocks), mean size of prey (larger on rocks), number of prey eaten (fewer on rocks) and microhabitat use (more restricted on rocks).

Gastrointestinal Helminths from Six Species of Frogs and Three Species of Lizards, Sympatric in Pará State, Brazil

Abstract Forty-three frogs representing 6 species (Dendropsophus cachimbo, Scinax fuscomarginatus, Leptodactylus fuscus, Leptodactylus martinezi, Leptodactylus mystaceus, and Leptodactylus rhodomystax) and 35 lizards representing 3 species (Kentropyx calcarata, Leposoma osvaldoi, and Potamites ecpleopus) collected in the Brazilian state of Pará were examined for helminths. One species of Trematoda, Brachycoelium salamandrae, and 12 species of Nematoda, adults of Capillaria recondita, Cosmocerca brasiliense, Cosmocerca podicipinus, Falcaustra belemensis, Falcaustra maculata, Kentropyxia sauria, Oswaldocruzia vaucheri, Physaloptera retusa, Schrankiana formulosa, Schrankiana fuscus, Schrankiana schranki, and juveniles of Acuariidae gen. sp., were found. Only B. salamandrae occurred in both frogs and lizards. There were 1.53 ± 0.13 (x ± 1 SE) helminth species/infected frogs and 28.52 ± 11.7 helminth individuals/infected frogs and 1.12 ± 0.08 helminth species/infected lizards and 6.47 ± 1.58 helminth individuals/infected lizards. Thirteen new host records and 2 new locality records are reported.

Ecological observations on cerrado lizards in Rondônia, Brazil

Although most of the state of Rondonia in western Brazil was recently covered by tropical forest, patches of two types of dry land habitats also are found and contain lizard species atypical of tropical forest. Anolis meridionalis, Micrablepharus maximiliani, Cnemidophorus sp., and Kentropyx vanzoi occurred in a typical cerrado grassland area in extreme southern Rondonia. Termite nests and armadillo burrows provide refuge for these cerrado lizards during widespread grass fires. Three morphotypes of at least two undescribed species of Tropidurus occurred on isolated granitic extrusions completely surrounded by tropical forest. Hoplocercus spinosus occurred on one of the extrusions. These islands of xeric habitat are not used by tropical forest species

Dietary asymmetry in leaf litter frogs and lizards in a transitional northern Amazonian rain forest

The use of food resources by two arthropodivorous groups of leaf litter vertebrates, frogs and lizards, was studied in a transitional tropical lowland forest in Roraima, Brazil. Nine species of frogs, represented primarily by small-bodied juveniles, and seven species of lizards, primarily small-bodied adults, composed the leaf litter fauna at the end of the wet season when the study was performed. Eighty-two prey categories, identified to family level, were recognized in the diets of these species of frogs and lizards. Overlaps in diet indicated little similarity among most species in prey types eaten, although a well-defined termite-ant guild composed of two species was identified. Ants, insect larvae, beetles, and termites contributed most to diets of all species combined, but frogs typically consumed more ants than lizards. As a group, frogs ate smaller prey than lizards, even when prey sizes were adjusted for body size. Frogs in general contained more prey than lizards (21.7 items per frog compared to 6.7 items per lizard) and had significantly larger stomach content volumes than lizards, indicating a major divergence in the basic strategy of food gathering between frogs and lizards. Frogs may have evolved relatively larger gut storage capacity to offset extended food shortages associated with prolonged inactivity during drought. However, differences in consumption of ants by frogs and lizards may relate to differences in defense strategies between the two groups. All amphibians have integumentary granular glands, which secrete many different compounds used in defense. Ants produce a variety of toxins, and some evidence in one lineage of frogs suggests that frogs may incorporate toxins into their skin from insects in their diets. Future work may elucidate whether lizard dietary choice has evolved to optimize energy intake whereas frog dietary choice has evolved to optimize uptake of chemicals important for defense.

Ecology of Whiptail Lizards (Cnemidophorus) in the Amazon Region of Brazil

We compared microhabitat use, morphology, diets, and reproduction in three populations of Cnemidophorus lemniscatus (Alter do Chio, Curua-Una, and Roraima) and one population of C. cryptus (Rio Xingu) in the Amazon region of Brazil. Cnemidophorus lemniscatus were most common in grasslands or other open areas, but C. cryptus was restricted to sandy beach. A greater percentage of C. cryptus than C. lemniscatus were observed foraging. Morphologically, C. lemniscatus populations were identical. Females of C. cryptus (all-female species) were larger than females of C. lemniscatus. Based on numerical occurrence of prey, diets of C. lemniscatus from Alter do Chao and Curua-Una were more specialized than those for C. lemniscatus from Lavrado or C. cryptus from the Rio Xingu. Based on volumetric occurrence of prey, C. lemniscatus from Alter do Chao were most specialized, feeding primarily on fruits of one plant species. Also based on volumetric data, diet of C. lemniscatus from Curua-Una was most similar to that of C. cryptus. Lizards from Alter do Chao and Curua-Una ate larger prey than did those from the other two sites. Concordandy, lizards in these two populations ate fewer prey. Clutch size varied from one to four eggs in C. lemniscatus and from one to two eggs in C. cryptus, and there was a significant relationship between female size and clutch size. Ecological variation exists among populations of Amazonian Cnemidophorus. Overall, there were no ecological differences that could not be explained simply on the basis of habitat or resource differences among localities.

Demography and Life History of Two Species of Chorus Frogs (Anura: Hylidae) in South Carolina

The demography and life history of two populations of two species of chorus frogs (Pseudacris ornata and P. nigrita) were studied for 4 yr on the Savannah River Plant near Aiken, South Carolina. Sexual maturity in both species is reached within the first year of life, and the population turnover is nearly annual. The sex ratio of adults that entered the breeding ponds each year at each locality was 1:1. The operational sex ratio was skewed toward males during the first breeding peak in P. ornata, but was 1:1 in P. nigrita. All females that entered the ponds for the first time were gravid, but the percentage of females depositing eggs within a season and within localities was variable. In general, when the number of adults breeding in one year was low, survival of these adults to the next breeding season was high, suggesting that there may be a cost to reproduction in terms of survival. Juvenile recruitment was highest in the wettest year of the study. Recruitment of P. nigrita was never as high as that of P. ornata. One of the study sites had an artificially lowered water level, and juvenile recruitment of P. ornata was low during all years at this site compared to the other pond. These species best fit a bet-hedging model of life history tactics. The breeding habitat is unpredictable in time and space. Juvenile mortality is predictably high, but where and when it occurs is random. Selection apparently has favored juvenile dispersal as an alternative to longevity and iteroparity of individual females.

A NEW AMAZONIAN SPECIES OF COLOSTETHUS (ANURA: DENDROBATIDAE) WITH A NIDICOLOUS TADPOLE

We describe adults, tadpoles, and vocalization of a new Amazonian species of Colostethus from a terra firme rainforest locality south of the Amazon River near Manaus, Amazonas, Brazil. This species is characterized by the absence of dorsolateral and ventrolateral stripes, the presence of a short, diffuse oblique lateral stripe, Finger III of male not swollen, and the presence of a black or gray throat in the male. In addition, the new species is larger than three other species in the Amazon region (C. caeruleodactylus, C. marchesianus, and C. stepheni) and its call, typically composed of long bouts of continuous notes, is distinct from these three species. This species is the fourth known Colostethus with an endotrophic tadpole; in three of these species, including C. nidicola, eggs are deposited and develop entirely in a terrestrial nest. Clutches of C. nidicola are composed of about three eggs and are placed in leaf litter on the forest floor. Whether C. nidicola is closely related to any of the other three species with endotrophic tadpoles is unknown at present. A phylogenetic analysis of this group of frogs will be necessary to detect whether endotrophy has evolved once or multiple times. Examination of tadpoles of C. nidicola and comparisons with characters reported for the other three species that have endotropic tadpoles revealed that tadpoles within each species have unique combinations of characters or loss of characters. Endotrophic tadpoles have not been reported for any other dendrobatids. Resumo Neste estudo nós descrevemos os adultos, os girinos e a volcalização de uma nova espécie de Colostethus da Amazônia central, de uma localidade de floresta tropical de terra firme ao sul do rio Amazonas, próxima a Manaus, Amazonas, Brasil. Essa espécie é caracterizada pela total ausência de faixas dorsolaterais e ventrolaterais, pela presença de uma curta e difusa faixa lateral oblíqua. Os machos apresentam o dedo III não dilatado e coloração preta ou cinza na região gular. Além disso, a nova espécie é maior que as outras três da região amazônica brasileira, C. caeruleodactylus, C. marchesianus, e C. stepheni, da quais difere tambén quanto a vocalização, com um canto, tipicamente composto de uma longa série de notas contínuas. Essa é a quarta espécie conhecida de Colostethus com um girino endotrófico; em três delas, incluindo C. nidicola, os ovos são depositados em um ninho terrestre onde se desenvolvem por completo. Ninhadas de C. nidicola são compostas de cerca de três ovos, geralmente colocados no folhiço do chão da floresta. Ainda não se sabe se C. nidicola é mais próximo de qualquer uma das outras três espécies com girinos endotróficos. Uma análise filogenética é necessária para detectar se a endotrofia surgiu uma ou mais vezes no grupo. A observação dos girinos de C. nidicola e sua comparação com características previamente atribuídas às outras três espécies com girinos endotróficos mostraram que os girinos de cada uma das espécies possuem uma combinação única de presença ou ausência de caracteres. Girinos endotróficos não foram encontrados em nenhum outro dendrobatídeo.