Martha Patricia Ramírez-Pinilla

Invasive Cells in the Placentome of Andean Populations of Mabuya: An Endotheliochorial Contribution to the Placenta?

New world lizards of the genus Mabuya have the most specialized level of placentotrophy among reptiles known to date, and related to that, they have the most complex allantoplacenta characterized by a series of morphological specializations that converge with those known for eutherian mammals. One of these specializations is the placentome that is found in the embryonic pole of the incubation chamber. In the mature allantoplacenta, this structure is morphologically the most complex, which could support an important amount of nutrient exchange between mother and fetus. According to the relationship between the chorioallantois and the syncytial uterine epithelia, the placenta of Mabuya populations shows some interesting similarities to the synepitheliochorial type. Recently, cells of chorionic origin have been found invading the syncytial uterine epithelium, and in very close proximity with uterine blood vessels. In this study, we describe the relationship between these invasive chorionic cells, the uterine syncytium, and the subjacent blood vessels of several populations of this genus, by means of high resolution optical microscopy and transmission electron microscopy. Cell groups originating from the chorion, of variable size and shape, penetrate the uterine syncytial epithelium extending complex cytoplasmic projections that come in contact with uterine capillaries and form an extensive and complex double‐membrane system that surrounds the capillary. The close relationship between the chorion and the maternal circulation suggests that the Mabuya placentome shows some characteristics of an endotheliochorial placenta. This finding constitutes so far the only documented example of an endotheliochorial placentation in Reptilia. Anat Rec, 2007.

Diet of the Andean Frog Ranitomeya virolinensis (Athesphatanura: Dendrobatidae)

Abstract The effects of sex, ontogeny, and season on the diet of Ranitomeya virolinensis were studied over one year. The diet of this Andean species is composed mainly of small prey; the most important prey categories according to index of relative importance (IRI) were Acari, Formicidae, Holometabolous larvae, and Collembola. There were no differences in total prey gut content over time assessed in number and volume; however, the diet composition of this Santander Poison Frog changed between dry and wet seasons, with Formicidae, holometabolous larvae and Collembola as the prey categories that contributed most to the difference. Males had fewer prey in their guts than females, but there were no compositional differences between sexes. There was a shift in the importance of prey caused by ontogeny. Mean prey volume increased with body size, whereas the occurrence of Acari and Formicidae varied inversely with SVL. Formicidae was the second most important prey category according to IRI. Therefore it is an important category as has been described previously for other Dendrobatid species. However, its importance fluctuated with the season. Acari was the most significant prey type in R. virolinensis as is the case for other small related species of the genus, although its importance changed with the ontogeny. The diet of this frog had a substantial phylogenetic component because closely related species have similar diets; nevertheless, its diet is clearly affected by other intrinsic and extrinsic factors.

Reproduction of an Introduced Population of Eleutherodactylus johnstonei at Bucaramanga, Colombia

Abstract Comparative ecological data on introduced populations can contribute to understanding why Eleutherodactylus johnstonei is a good invader. We studied the reproductive features of an introduced population of this species and compared them with similar data on other introduced and native populations. Females were larger than males; sexually mature males ranged between 17–29 mm snout vent length and females between 23–32 mm. Reproductive males and females were captured throughout the year and there were no monthly significant differences in their occurrence. Clutches and neonates occurred year-round. The adjusted testicular volume did not vary significantly among months and histological analyses of the testes and ducts revealed the presence of sperm through the year, indicating continuous reproductive activity for males. The ovarian volume did not vary significantly among months and the presence of yolked follicles were observed throughout the year, indicating that females also reproduce continuously. There was a positive relationship between female body size and the number of yolked follicles. Two different relationships associated with reproduction could explain sexual differences in body size; the larger body size in females allows greater clutch sizes, and the energy cost of calling activity and paternal care of the clutch limits male growth. The colonizing success of E. johnstonei appears to be related to its reproductive features, such as flexibility in reproductive activity, direct development, and parental care of the clutch, allowing it to easily occupy disturbed areas that it encounters.

Morphological Variation in the Allantoplacenta Within the Genus Mabuya (Squamata: Scincidae)

The type IV allantoplacenta has been described for the New World tropical scincids lizards of the genus Mabuya; it possesses the greatest morphological complexity known among viviparous squamates. Although a common morphological pattern has been observed in the few species of this lineage in which the allantoplacental morphology has been studied, some morphological variations may be present among species and populations. Here, we report morphological variation of the allantoplacenta of twelve populations of the genus Mabuya distributed in different geographical areas in northern South America using light microscopy. It is found that all the populations/species conserve a general arrangement of the placental structures. In the embryonic hemisphere there are a placentome, paraplacentome, and chorionic areolas; these structures are related to histotrophic nutrition. At the abembryonic hemisphere, there are absorptive plaques for histotrophic transfer and respiratory segments for gas exchange. However, in some populations some distinctive features in the placentome were found. The presence in the uterine syncytium of non syncytialized columnar cell groups, and invasive cells and apical projections of the chorionic cells directed toward the uterine syncytium, constitute a localized endotheliochorial placenta. Likewise, variations found in the abembryonic region include a greater morphological complexity, such as the folded and delimited absorptive plaques, and highly folded regions at the abembryonic pole (folded respiratory segments integrated with folded absorptive plaques). These specializations allow a larger surface for the passage of nutrients and respiratory exchange. Replication and the regionalized differentiation of the absorptive plaques were probably instrumental in the emergence of specialized structures for nutrient transport such as the placentome and the different types of absorptive plaques. These developmental processes appear to underlie the evolution of the placental complexity within thegenus Mabuya by the morphological variation of serial homologous structures. Anat Rec, 291:1124–1139, 2008.

Uterine and chorioallantoic angiogenesis and changes in the uterine epithelium during gestation in the viviparous lizard, niveoscincus conventryi (Squamata: Scincidae).

We used immunofluorescent confocal microscopy and scanning electron microscopy to quantify uterine vascularity and to describe uterine surface morphology during gestation in pregnant females of the lecithotrophic lizard Niveoscincus coventryi. As uterine angiogenesis and epithelial cell morphology are thought to be under progesterone control, we studied the effect of a progesterone receptor antagonist (mifepristone) on uterine and chorioallantoic microvasculature and features of the uterine epithelial surfaces. Although intussuceptive angiogenesis was observed in both, uterine and chorioallantoic, vascular beds during gestation, the only significant increases were in the diameters of the uterine vessels. An ellipsoid vessel‐dense area grows in the mesometrial hemisphere of the developing conceptus, which parallels the expansion of the allantois to form the chorioallantoic placenta. Uterine surface topography changed during gestation. In particular, uterine blood vessels bulge over the luminal surface to form marked ridges on the uterine embryonic hemisphere, especially during the last stage of pregnancy, and ciliated cells are maintained in the embryonic and abembryonic hemispheres but disappear in both the mesometrial and antimesometrial poles. This distinct regionalization of uterine ridges and ciliated cells in the uterine surface and in the shape of the epithelial component of the chorion might be related to the function of both chorioallantoic and yolk sac placentae during gestation. There was no significant difference between females treated with or without mifepristone, which may be related to the partial function of mifepristone as a progestin antagonist and/or with the function and time of action of progesterone in the uterus during gestation in N. coventryi. Differences in the pattern of angiogenesis and uterine surface morphology during gestation among squamates may be related to the functional diversity of the uterine component of the different placentae and probably reflect its diverse evolutionary history. J. Morphol., 2011.

Diet, microhabitat use, and thermal preferences of Ptychoglossus bicolor (Squamata: Gymnophthalmidae) in an organic coffee shade plantation in Colombia

Ptychoglossus bicolor es un pequeno lagarto de la familia Gymnophthalmidae, que habita el valle del Rio Magdalena de Colombia. Se estudiaron las caracteristicas ecologicas de la dieta, uso de microhabitat y preferencias termales de una poblacion que habita una plantacion de cafe organico bajo sombra en la Cordillera Oriental colombiana. La dieta en esta poblacion esta dominada por isopodos. El Indice Valor de Importancia Relativa fue del 98.8% y no hubo diferencias mensuales significativas en el contenido estomacal y el volumen de isopodos consumidos durante el ano, ni tampoco entre las estaciones de lluvia y seca. Un gran numero de lagartos fueron encontrados activos entre la hojarasca, enterrados junto a las raices de los arboles y bajo o dentro de troncos en descomposicion. La temperatura corporal estuvo positivamente correlacionada con las temperaturas del suelo y del aire y no hubo diferencias significativas en temperatura corporal entre los sexos. En esta localidad no encontramos lagartos fuera de los campos de cultivo de cafe. Nuestros resultados sugieren que estos lagartos sobrellevan exitosamente las condiciones ofrecidas por los cafetales organicos como resultado del sistema de cultivo. Asi, esta poblacion podria ser vulnerable a cualquier modificacion del habitat que cambie la disponibilidad de microhabitats y la abundancia de isopodos.

Reproductive Activity of Three Sympatric Viviparous Lizards at Omiltemi, Guerrero, Sierra Madre del Sur, Mexico

Abstract We studied the reproductive characteristics of sympatric populations of Sceloporus formosus scitulus, Sceloporus omiltemanus (Phrynosomatidae), and Mesaspis gadovii (Anguidae) at the Omiltemi forest reserve (Guerrero, Mexico). Males are larger and reach larger body sizes at reproductive maturity and are more colorful than females in both Sceloporus, whereas males are smaller than females and reach sexual maturity at similar body sizes in M. gadovii. These species are single brooded and follow a common pattern of annual reproductive activity. The reproductive activity of females and males of the three species is seasonal; vitellogenesis is initiated in late summer and continues in autumn/rainy season, gestation occurs throughout the winter/dry season, and parturition occurs in early spring. All three species have intersexual synchrony in reproductive activity. In spite of similar reproductive schedules, some subtle features related to the length of each of the reproductive stages could be observed. Sceloporus formosus scitulus has a more extended reproductive season, and large females start vitellogenesis earlier than do small ones. Males have a prolonged reproductive activity and a short nonreproductive season. In contrast, the reproductive cycle of the other two species is defined by shorter reproductive season and less intrasexual asynchrony for both sexes than found in S. f. scitulus. The seasonal pattern of reproduction shared by these three species is characteristic of other viviparous lizards at high elevations in tropical and subtropical latitudes of Central and South America, being convergent for different lizard families. This convergence in reproductive patterns suggests a common evolutionary response to environmental factors associated with montane habitats, whereas specific differences observed within species are attributed to the particular evolutionary history of each taxon.

How does diet influence the reproductive seasonality of tropical freshwater fish?: A case study of a characin in a tropical mountain river

Seasonal breeding of tropical freshwater fish may be synchronized with periods of high food consumption. We explored this hypothesis by studying the relationship between diet and reproductive activity of Creagrutus guanes (Teleostei, Characidae). Our results showed that C. guanes had a generalist and omnivorous diet dominated by aquatic insects (mainly Diptera larvae) and seeds. Creagrutus guanes did not show intersexual or ontogenetic variation in diet. Peaks of feeding activity during rainy months were not synchronized with breeding in dry months. Our results do not support the hypothesis that the reproductive season has to be synchronized with high food consumption. We discussed the hypothesis fat reserves may be an important factor for the desynchronization of peaks of feeding and reproduction as explanation of seasonal breeding of this species.

Microhabitats for Oviposition and Male Clutch Attendance in Hyalinobatrachium aureoguttatum (Anura: Centrolenidae)

In this study we describe for the first time aspects of the reproductive ecology and behavior of a population of Hyalinobatrachium aureoguttatum located in the Colombian Pacific lowlands. Males vocalize and attend clutches from the underside of leaves overhanging the streams. Males showed high fidelity to their territory; each male repeatedly uses the same leaf for perching, calling, mating, and clutch attendance. There were no significant differences in the environmental variables registered for the microhabitats where males were located with or without clutches, with one or multiple clutches, or between successful or unsuccessful clutches, which suggest that the analyzed variables are not important for the obtention of the clutches and their success. Males were found grouped in the study area at distances varying between 0.3–0.5 m; thus, more than one male can be observed occupying other leaves in the same plant. Fights or aggressive behaviors were not observed in intrusion events by co-specific males in the territory of the resident males; however, we registered a series of movements that resulted in moving the intruder further away. Females almost immediately abandoned the clutches after oviposition, whereas most of the time, at day and night, males stayed near, touching or sitting on one to five egg clutches during most of their embryonic development. This brooding behavior also included hydration, cleaning, and defense of the eggs. Arthropod predation was observed in both attended and abandoned egg clutches; however, in one observation, the behavior of the male moved the predator away and saved the clutch. These observations and the finding of abandoned clutches that did not complete their development suggest that male parental care increases embryo survival and, as a result, his reproductive success.

Limb development in the gekkonid lizard gonatodes albogularis: A reconsideration of homology in the lizard carpus and tarsus

Despite the attention squamate lizards have received in the study of digit and limb loss, little is known about limb morphogenesis in pentadactyl lizards. Recent developmental studies have provided a basis for understanding lizard autopodial element homology based on developmental and comparative anatomy. In addition, the composition and identity of some carpal and tarsal elements of lizard limbs, and reptiles in general, have been the theme of discussions about their homology compared to non‐squamate Lepidosauromorpha and basal Amniota. The study of additional embryonic material from different lizard families may improve our understanding of squamate limb evolution. Here, we analyze limb morphogenesis in the gekkonid lizard Gonatodes albogularis describing patterns of chondrogenesis and ossification from early stages of embryonic development to hatchlings. Our results are in general agreement with previous developmental studies, but we also show that limb development in squamates probably involves more chondrogenic elements for carpal and tarsal morphogenesis, as previously recognized on the grounds of comparative anatomy. We provide evidence for the transitory presence of distal carpale 1 and intermedium in the carpus and tibiale, intermedium, distal centralia, and distal tarsale 2 in the tarsus. Hence, we demonstrate that some elements that were believed to be lost in squamate evolution are conserved as transitory elements during limb development. However, these elements do not represent just phylogenetic burden but may be important for the morphogenesis of the lizard autopodium. J. Morphol., 2010.