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The first section of this perspective explains how my early years shaped my thought processes, how I was shoved into academia, and how I stumbled onto a track to employment, tenure, and retirement at a single university. I always sought a broad education to support studies of mostly descriptive biology that were driven by my curiosity and the diversity of the amphibian life cycle. In that regard, I experienced the benefits of being gainfully employed without just having a job. The second section highlights my graduate students, collaborations, and research focus on larval amphibians at Mississippi State University. I felt it was my responsibility to prepare undergraduate and graduate students for their choices of life's pursuits. At the end, I try to think about the future study of larval amphibians, and based on technological advances and the sporadic insights of a few lucky persons, I am optimistic about what will happen.
Reproductive aspects of most snake species remain elusive because of secretive habits or rarity. Here, we report data on litters of Crotalus triseriatus from two populations in central Mexico. We made 4-d visits to both study sites every other week from April to June during 2014 and 2015 (Site 1) and during 2015 (Site 2). Surveys were made from 0900 to 1800 h to catch as many gravid females as possible. All adult females were maintained in captivity until parturition. We recorded a total of 16 litters (10 from Site 1 and six from Site 2). Average litter size was 7.2 ± 2.2 (n = 13), higher than previously reported in the species. We found no relationship between maternal snout–vent length (SVL) and litter size, and litter size did not differ between study sites or years. In contrast with other studies, we found no relationship between neonate SVL, body mass, and litter size or between maternal and neonatal traits. Dusky Rattlesnakes demonstrate a plastic reproductive response to changing environmental conditions. Neonate body size varied between sites, indicating that local selection may act through predation pressure, prey availability, or other environmental variables. Local selection may lead to differences in life history traits, whereas annual variation in factors such as prey availability might influence reproductive traits. Our study highlights the need for long-term studies to understand the sources of variation in life history.
Los atributos reproductivos de la mayoría de las especies de serpientes permanecen desconocidos debido a sus hábitos sigilosos o a su rareza. En este estudio reportamos datos sobre camadas de Crotalus triseriatus de dos poblaciones del centro de México. Hicimos visitas de cuatro días a ambos sitios de estudio cada dos semanas desde abril a junio en 2014 y 2015 (Sitio 1) y en 2015 (Sitio 2). La búsqueda se realizó de 0900 a 1800 h para capturar tantas hembras grávidas como fuera posible. Todas las hembras adultas se mantuvieron en cautiverio hasta el parto. Registramos un total de 16 camadas (10 del Sitio 1 y seis del Sitio 2). El tamaño promedio de camada fue de 7.2 ± 2.2 (n=13), mayor que el que se había reportado anteriormente. No existe una relación entre la longitud hocico-cloaca (LHC) de la madre y el tamaño de camada. No existieron diferencias significativas en el tamaño de camada entre los sitios de estudio y entre años de estudio. En contraste con otros estudios, no encontramos relación entre la longitud hocico-cloaca de los neonatos, la masa corporal y el tamaño de camada o relaciones entre los atributos de los neonatos y los atributos maternos. Crotalus triseriatus muestra una respuesta plástica en su reproducción a los cambios en las condiciones ambientales. La talla de los neonatos varió entre sitios, indicando que las fuerzas selectivas locales pueden actuar a través de las presiones de depredación, disponibilidad de presas u otras variables ambientales. La selección local puede llevar a diferencias en los atributos de historia de vida, mientras que la variación anual en los factores ambientales como la disponibilidad de presas puede influir sobre los atributos reproductivos. Nuestro estudio resalta la necesidad de estudios a largo plazo para entender las fuentes de variación sobre los atributos de historia de vida.
Few studies have characterized the reproductive cycles of desert anurans, particularly species from South America. This has hampered efforts to identify broad patterns in anuran reproduction, which are known to vary both phylogenetically and throughout climatic gradients. We studied the reproductive cycle of male Odontophrynus barrioi, a small (∼20 g) terrestrial toad from the Monte Desert of San Juan, Argentina. The main goal of this work was to determine spermatogenic activity, plasma testosterone concentrations, and reproductive parameters during prereproductive (preR), reproductive (R), and postreproductive (postR) periods. We determined the plasma testosterone concentrations in male toads by radioimmunoassay (RIA). We performed histological analyses of the testes of males with the use of the hematoxylin and eosin method, and also examined the testes with a light microscope. During the preR and R periods, spermatogenesis in O. barrioi showed substantial development of the late stages (sperm bundles), coincident with high sperm percentage (spermiation) in the seminiferous tubules. Spermiation occurred when testosterone levels were high. This species exhibits a continuous spermatogenic cycle, with maximum levels of testosterone during the dry season. Therefore, O. barrioi is a desert-adapted anuran exhibiting an “associated” reproductive strategy given its association between breeding season and high plasma testosterone concentrations. This reproductive strategy likely evolved to coordinate the reproductive cycle with brief rains in summer as an adaptation to the challenging climate imposed by the desert environment, as well as Monte Desert.
There are few studies of animal communities in coastal zones, especially those of herpetofauna. We conducted herpetofaunal surveys in open shoreline habitats for 3 yr in three large protected areas in the Mixedwoods Plains Ecozone of the southern Laurentian Great Lakes. These locations are isolated preserves in one of the most heavily human-modified areas of North America. We found 17 species with low to moderate similarity of species membership and highly uneven relative abundance and biomass. Common Five-Lined Skinks dominated communities in relative abundance, dominated biomass at one location, and codominated biomass with Common Gartersnakes and Eastern Foxsnakes or Milksnakes at the other two locations. Five other species also regularly inhabited the coastal zone, whereas others were more transient users. Review of species' dietary requirements suggest that consumption of arthropods and other invertebrates may play an important role in structuring the community. Both the legacy of historical and more recent anthropogenic changes have altered the structure of these communities into “novel ecosystems.” Further study of coastal herpetofaunas and their functional role in ecosystems is warranted.
From the 1950s to the present, many researchers have tested time series data for density dependence. All kinds of organisms have been studied, from microorganisms to insects and vertebrates to plants. A variety of techniques and population growth models were developed, and the conceptual framework to study populations has been improved. We searched for long time series data on amphibians and reptiles in the literature. From 102 population time series, and after filtering the dataset, we tested for density dependence in time series data for 69 populations (52 species) of amphibians (anurans and caudatans), serpents, lacertilians, chelonians, rhynchocephalians, and crocodilians. We used the exponential growth state-space model and the Ornstein-Uhlembeck state-space model as proxy models for density-independent and density-dependent population growth models, selecting between them with the parametric bootstrap likelihood ratio test. The hypothesis of density independence was rejected for 2 amphibians, 11 serpents, 3 chelonians, 1 rhynchocephalian, and 2 crocodilian populations. Detailed data for serpents and chelonians allowed identification of external factors such as changing food supplies and habitats as drivers of observed changes in population densities. We highlight the need of both long-term and experimental studies on reptile and amphibian populations in semipristine or preserved areas.
Desde los años 50s hasta nuestros días, diversos investigadores han puesto a prueba denso-dependencia en series temporales de datos. Todo tipo de organismos han sido estudiados, desde microorganismos a insectos, vertebrados y aves. Una variedad de técnicas y de modelos de crecimiento poblacional se han desarrollado, e incluso el marco conceptual de estudios poblacionales fue mejorado. Realizamos búsquedas de datos en series temporales largas para reptiles y anfibios en la literatura. De las 102 poblaciones encontradas y luego de filtrar la base de datos, analizamos 69 poblaciones (52 especies) de anfibios (anura y caudata), serpientes, lagartos, tortugas, tuatara, alligators y caimanes. Utilizamos exponential growth state-space y Ornstein-Uhlembeck state-space como aproximación a los modelos de crecimiento poblacional denso-independiente y denso-dependiente, seleccionando entre ellos por medio del parametric bootstrap likelihood ratio test. La hipótesis de denso-independencia fue rechazada para poblaciones de 2 anfibios, 11 serpientes, 3 tortugas, 1 tuatara, 1 alligator y 1 caimán. Información detallada disponible para las poblaciones de serpientes y tortugas permitieron identificar factores externos (como cambios en el alimento disponible y en el hábitat) como responsables de los cambios observados en las densidades poblacionales. Resaltamos la necesidad tanto de estudios a largo plazo o experimentales, en poblaciones de anfibios y reptiles en áreas semiprístinas o preservadas.
The detrimental effects of parasite infection include modulation of behaviors important to host fitness. The Mink Frog, Lithobates septentrionalis, is the final host of the digenean flatworm, Halipegus eccentricus, which inhabits the eustachian tube. Extreme infection results in complete occlusion of the eustachian tubes and could adversely affect a frog's hearing. The tympanic membranes are coupled internally through the buccal cavity via open eustachian tubes, making them vulnerable to pressure changes induced by obstruction from the presence of H. eccentricus, accumulated necrotic tissue, and mucus resulting from the infection. We tested phonotactic response in male L. septentrionalis to determine whether acoustic response is affected by infection of H. eccentricus. We placed frogs, in turn, in a floating choice arena, gave them 10 min to acclimate and 10 min to respond to a conspecific advertisement call broadcast from a speaker. We tracked the frogs and recorded positive phonotaxis when the frog approached the broadcast speaker. We measured individual frogs, checked them noninvasively for infection, and released them at the capture site. Infection rates were moderate: 43% of males had at least one H. eccentricus in one or both sides. Parasite infection significantly affected phonotaxis response; parasite-free males exhibited significantly more, and parasitized males significantly fewer, positive responses than expected. Although response measures, including time to response, did not differ significantly between the two groups of males, this behavioral assay provides good evidence that infection by H. eccentricus affects a frog's ability to localize and respond to a conspecific call.
The growth rate of reptiles is plastic and often varies among individuals, populations, and years in response to environmental conditions. For an imperiled species, the growth rate of individual animals is an important component of demographic models, and changes in individual growth rates might precede changes in abundance. We analyzed a long-term dataset on the growth of Giant Gartersnakes (Thamnophis gigas) to characterize spatial and temporal variability and evaluate potential environmental predictors of growth. We collected data on the growth in snout–vent length (SVL) of Giant Gartersnakes over 22 yr (1995–2016) from eight sites distributed throughout the Sacramento Valley of California, USA. The von Bertalanffy growth curves indicated male Giant Gartersnakes grew faster toward shorter, asymptotic SVL than did females. Nearly equal variability in growth was attributable to differences among years and among sites. From 2003–2016 we collected data on precipitation, temperature, and the abundance of fish and anuran prey at each site and used these variables as predictors in growth models of Giant Gartersnakes. Snake growth was positively related to the amount of precipitation that fell during the prior water year and the abundance of anurans at a site. Fish and frog abundance interacted to affect snake growth: at low abundances of one prey type, the other positively affected growth, but the slope of this relationship decreased as alternative prey abundance increased. Our results highlight the plasticity of growth in this threatened snake species, point to potential environmental drivers of growth, and provide valuable data for demographic modeling efforts.
A new species of Leposternon is described from the Brazilian Cerrado, with records from the municipalities of Buritizeiro and João Pinheiro, state of Minas Gerais, central Brasil. The new species has precloacal pores and pectorals scales mostly diamond shaped, and these characteristics distinguish it from all congeners except Leposternon cerradensis, Leposternon kisteumacheri, Leposternon maximus, and Leposternon polystegum. It differs from the pored Leposternon species by a combination of external morphology and dental features. The morphology of the new species is similar to other species of the genus Leposternon with precloacal pores.
Uma nova espécie de Leposternon é descrita do Cerrado brasileiro, com registros em Buritizeiro e João Pinheiro, Minas Gerais, Brasil. A nova espécie pode ser distinguida dos demais congêneres, exceto de Leposternon cerradensis, Leposternon kisteumacheri, Leposternon maximus e Leposternon polystegum, por ter poros pré-cloacais e a maioria das escamas peitorais com formato de diamante. A espécie nova difere das espécies do gênero Leposternon com poros pré-cloacais por uma combinação de atributos da morfologia externa e características dentárias. A morfologia da nova espécie é similar à de outras espécies do gênero Leposternon com poros pré-cloacais.
Northern Map Turtles, Graptemys geographica, are a long-lived riverine species of conservation concern. We examined carapace morphology of Northern Map Turtles at Mount Union, a major turtle nesting area and former industrial site along the Juniata River in central Pennsylvania, USA. Among 535 reproductive adult female G. geographica, 29% exhibited abnormal shell shape, often in the form of an indentation in one or both sides of the carapace. Older females had a higher incidence of abnormalities than younger females. We quantified variation in shell shape, compared morphology among life history stages, and assessed thermal incubation environments of embryos to determine the magnitude and potential source of shell shape abnormalities. Geometric morphometric analysis showed significant differences among several carapace shape categories of adult turtles. No shell shape abnormalities were observed among 703 hatchlings collected from nests, and no shell shape abnormalities were observed among seven of those marked hatchlings that returned to Mount Union as 11- to 18-yr-old adult females to nest. Historically, most of the nesting substrate at Mount Union consisted of black coal tailings, which exposed developing embryos to high temperatures and potential chemical insults. The high incidence of abnormal carapace shapes of adult female Northern Map Turtles at Mount Union may reflect a delayed morphological response to chemical or thermal conditions encountered in the nesting substrate, direct exposure to contaminants in the Juniata River as subadults, or factors that affected turtles a generation ago but have since abated.
Melanic pigments play a key role in the coloration of animals, but the type of melanin pigment in black, brown, and blue colored scales of Squamata has not been studied. Based on research on birds and mammals, we may expect that pheomelanin is the majority pigment in brownish colorations and eumelanin is the majority pigment in black and blue colorations of Squamata. To characterize the pigments that underlie the melanin-based colorations of lizards, we analyzed the skin of nine genera of lacertids using dispersive Raman spectroscopy. Our results suggest that no prediction can be made on the type of pigmentary melanin present in the skin of the lacertids based alone on the hue of the sample. Indeed, brownish patterns in the skin of Psammodromus, Gallotia, Acanthodactylus, and Algyroides lizards presented both chemical forms of melanin: eumelanin and pheomelanin. Therefore, pheomelanogenesis might be an ancient characteristic within Lacertidae, because it was detected in genera in the Lacertini, Eremini, and Gallotini. Raman spectra of melanic-based patterns of genus Zootoca and ultraviolet (UV)-blue patches of Podarcis, Iberolacerta, Lacerta, and Timon lizards suggested that eumelanin is the majority pigment in these patches. Raman spectroscopy is a suitable nondestructive technique useful to identify melanin forms in the skin of lizards, and it demonstrated that pheomelanin is synthesized by Squamata.
Los pigmentos melánicos juegan un papel clave en la coloración de los animales. Sin embargo, en los Squamata se desconoce la identidad molecular de los pigmentos melánicos (i.e., eumelanina y feomelanina) responsables de las coloraciones negras, marrones y azules. Basado en estudios anteriores en aves y mamíferos, cabría esperar que la feomelanina fuera el pigmento mayoritario en coloraciones marrones y que la eumelanina sea el pigmento mayoritario en las coloraciones negras y azules de los Squamata. Para caracterizar los pigmentos responsables de la coloración melánica en lagartos hemos analizado la piel de nueve géneros de lacértidos usando espectroscopía Raman dispersiva. Nuestros resultados sugieren que no se puede predecir el tipo de melanina pigmentaria presente en la piel de los lácertidos basándonos solo en la tonalidad de la muestra. De hecho, en los patrones de color marrón de la piel de lagartos de los géneros Psammodromus, Gallotia, Acanthodactylus y Algyroides están presentes ambas formas químicas de la melanina pigmentaria, es decir, eumelanina y feomelanina. En los patrones melánicos del género Zootoca y en las manchas ultravioleta (UV)-azules de lagartos en los géneros Podarcis, Iberolacerta, Lacerta, y Timon el espectro Raman sugirió que la forma eumelánica debe de ser el pigmento mayoritario en estas manchas. La espectroscopía Raman es una técnica no destructiva que es aplicable para identificar las formas melánicas presentes en la piel de los lagartos y demostró que los Squamata pueden sintetizar feomelanina.
Vertebrates respond to seasonal changes and environmental stressors by modulating their circulating glucocorticoid levels. Fluctuations in glucocorticoids alter various aspects of an organism's physiology and mediate behaviors such as appropriate reactions to unexpected threats or to expected annual challenges such as reproduction. This study examined corticosterone, the most important glucocorticoid in reptiles, levels in gravid and postoviposition adult female Painted Turtles (Chrysemys picta) during the reproductive season to understand how circulating glucocorticoid levels change with reproductive status. Gravid females exhibited higher levels of circulating corticosterone for both baseline measurements and the stress response series. Understanding such endocrinological variation with reproductive status can provide additional insight into the role of corticosterone during the nesting process in freshwater turtles.
Habitat loss, land-use transformation, climate change, and biological invasions all elevate the importance of plasticity in food selection for the continued persistence of dietary specialists. Horned lizards (Phrynosoma spp.) are myrmecophagic specialists and the abundance of ant prey make their populations vulnerable to habitat loss, as well as invasive ants and associated pest control programs. We studied ant use by Phrynosoma cornutum (Texas Horned Lizards) on an insular urban reserve in central Oklahoma that was bereft of harvester ants (Pogonomyrmex spp.), presumed to be their chief prey. The five most commonly available ant genera based on bait station captures were Monomorium (69%), Forelius (11%), Pheidole (10%), Crematogaster (7%), and Tapinoma (2%). Based on the examination of 124 scat samples from adult and juvenile P. cornutum, Crematogaster (81%), Pheidole (12%), Formica (6%), and Monomorium (1%) were used as prey. Consumption of prey in several ant genera by P. cornutum disproportionately to their availability was related to ant mass and presumed nutritional value. Among juveniles, gape size did not influence Pheidole use but may influence Formica use. We suggest that P. cornutum are adaptive ant specialists whose populations might be maintained in habitat fragments without harvester ants as long as abundant medium- and large-sized native ant communities are present. Therefore, urban reserves, when effectively managed for native fauna, can conserve declining native species by serving as habitat havens in an otherwise unsuitable landscape.
Information on amphibian diversity in Neotropical savannas and in protected areas in the Caribbean is lacking. We evaluated amphibian diversity and species composition in the Aripo Savannas Scientific Reserve in Trinidad, in relation to the two major habitat types, savanna and marsh forest. Thirty 200-m-long transects were sampled visually and aurally in 4 periods (total 120 samples), with 10 transects in savanna, and 20 in marsh forest (10 along trails and 10 off trails), at night in the wet season from June to December 2015. We recorded 895 individuals representing 16 species, 11 genera, and 7 families, with greater counts and diversity of amphibians in marsh forest compared to savanna. The three species recorded in savanna (Leptodactylus fuscus, Scinax ruber, and Rhinella beebei) were also found in marsh forest, with no separate savanna amphibian community. Audio detection was more effective at sampling most species, and there were greater counts along trails compared to transects off trails.
We describe a new species of Tupinambis from central South America in a transitional region between Amazonia, Cerrado, and Pantanal. The new species differs from its congeners by the number of femoral pores, posterior gulars, and mesoptychial scales and by color pattern. It is partially sympatric with Tupinambis cuzcoensis, Tupinambis longilineus, Tupinambis quadrilineatus, and maybe also with Tupinambis teguixin, but in general terms they tend to substitute one another in space.
Descrevemos uma nova espécie de Tupinambis da região central da América do Sul, em uma área de transição entre Amazônia, Cerrado e Pantanal. A nova espécie difere das congêneres pelo número de poros femorais, escamas gulares posteriores, escamas entre as dobras antegular e gular, e padrão de coloração. É simpátrica com Tupinambis cuzcoensis, T. longilineus, T. quadrilineatus e tavez também com Tupinambis teguixin, mas em termos gerais essas espécies tendem a se substituir geograficamente.