Coping with drought? Effects of extended drought conditions on soil invertebrate prey and diet selection by a fossorial amphisbaenian reptile.

Arid climates are characterized by a summer drought period to which animals seem adapted. However, in some years, the drought can extend for unusually longer periods. Examining the effects of these current extreme weather events on biodiversity can help to understand the effects of climate change, as models predict an increase in drought severity. Here, we examined the effects of "unusual" extended drought on soil invertebrate prey availability and on diet composition (based on fecal contents) and diet selection of a fossorial amphisbaenian, the checkerboard worm lizard Trogonophis wiegmanni. Weather data show interannual variations in summer drought duration. The abundance and diversity of soil invertebrates in spring were high, and similar to those found in a "normal" early autumn, after some rain had ended with the summer drought. In contrast, in years with "unusual" extended drought, abundance, and diversity of soil invertebrates in early autumn were very low. Also, there were seasonal changes in amphisbaenians' diet; in autumn with drought, prey diversity, and niche breadth decreased with respect to spring and autumns after some rain had fallen. Amphisbaenians did not eat prey at random in any season, but made some changes in prey selection that may result from drought-related restrictions in prey availability. Finally, in spite that amphisbaenians showed some feeding flexibility, their body condition was lower in autumn than in spring, and much lower in autumn with drought. If extended drought became the norm in the future, amphisbaenians might suffer important negative effects for their health state.

Intersexual and body size-related variation in chemical constituents from feces and cloacal products involved in intraspecific communication of a fossorial amphisbaenian.

Background: Many animals rely on chemical cues for intraspecific communication. This is especially important in fossorial animals because visual restrictions of the underground environment limit the opportunities for visual communication. Previous experiments showed the ability of the amphisbaenian Trogonophis wiegmanni to discriminate between several categories of conspecifics based on chemical cues alone. However, in contrast with many other reptile species, T. wiegmanni does not have external secretory glands, but uses uncharacterized secretions from the cloaca in intraspecific chemosensory communication. Methods: Using gas chromatography-mass spectrometry (GC-MS), we analyzed the lipophilic compounds from feces and cloacal products freshly extracted from the cloaca of male and female T. wiegmanni. We identified and estimated relative proportions of the compounds found, and tested for intersexual and body-size related differences. Results: We found a total of 103 compounds, being some steroids (mainly cholesterol and cholestanol), some alkanes and squalene the most abundant and frequent. Further, we found intersexual differences, with males, especially larger ones, having higher proportions of several alkanes between C13 and C24 and of squalene than females, which had higher proportions of several steroids and also of nonacosane and methylnonacosane than males. We compared these findings with secretions of other animals and discuss the potential role of these compounds and their variations in intraspecific communication of amphisbaenians.

Relationships between soil pollution by heavy metals and melanin-dependent coloration of a fossorial amphisbaenian reptile.

Melanin is the basis of coloration in many animals, and although it is often used in communication, thermoregulation, or camouflage, melanin has many other physiological functions. For example, in polluted habitats, melanin can have a detoxifying function. Melanic coloration would help to sequester in the skin the heavy metal contaminants from inside the body, which will be expelled to the exterior when the skin is sloughed. Moreover, animals should have evolved more melanic colorations in more polluted habitats ("industrial melanism" hypothesis). We examined whether the fossorial amphisbaenian reptile, Trogonophis wiegmanni, is able to eliminate heavy metals, derived from soil pollution by seagull depositions, through sloughing its skin. Our results suggest a covariation between levels of soil pollution by heavy metals and the concentration of heavy metals in the sloughed skins of amphisbaenians. This suggests that amphisbaenians may expel heavy metals from their bodies when they slough the skins. We also tested whether amphisbaenians inhabiting soils with higher levels of heavy metal pollution had darker (melanin-dependent) body colorations. However, contrary to predictions from the "industrial melanization" hypothesis, we found a negative relationship between soil pollution and proportions of melanic coloration. This contradictory result could, however, be explained because heavy metals have endocrine disruption effects that increase physiological stress, and higher stress levels could result in decreased melanogenesis. We suggest that although amphisbaenians might have some detoxifying mechanism linked to melanin in the skin, this process might be negatively affected by stress and result ineffective under conditions of high soil pollution.

Going underground: short- and long-term movements may reveal the fossorial spatial ecology of an amphisbaenian.

BACKGROUND: The movement and spatial ecology of an animal depends on its morphological and functional adaptations to its environment. In fossorial animals, adaptations to the underground life help to face peculiar ecological challenges, very different from those of epigeal species, but may constrain their movement ability. METHODS: We made a long-term capture-recapture study of the strictly fossorial amphisbaenian reptile Trogonophis wiegmanni to analyze its long-term movement patterns. We also used passive integrated transponder (PIT) telemetry to detect and follow undisturbed individuals underground, obtaining data of their short-term movement patterns. RESULTS: Amphisbaenians showed a high site fidelity, moving short distances and over small areas, and spending some days without any noticeable movement, even under favorable conditions. We also found differences in movements between sexes and age classes. CONCLUSIONS: This movement and spatial strategy can be related to the energetic constrains of underground burrowing, or to the low metabolic requirements of fossorial reptiles, as distances and areas covered were much smaller than for epigeal reptiles of similar size. Individual differences probably reflect differential reproductive and social requirements of males and females, and that younger individuals might show more floating behavior until they can settle in a territory. This study is a rare example describing the movement ecology of a fossorial species and may contribute to the general understanding of the factors that affect space use and movement decisions in animals.

Offspring and adult chemosensory recognition by an amphisbaenian reptile may allow maintaining familiar links in the fossorial environment.

Kin recognition is a phenomenon with an important function in maintaining cohesive social groups in animals. Several studies have examined parent-offspring recognition in species with direct parental care. Few studies have, however, explored parent-offspring recognition in animals that, at best, only show apparent indirect parental care, such as some reptiles. In this study, we investigated reciprocal parent-offspring recognition in the fossorial amphisbaenian Trogonophis wiegmanni, a viviparous species that shows potential stable 'family groups' in the form of parent-offspring long-term associations. We examined whether adult males and females could discriminate via chemical cues between familiar juveniles which associate with them within their family groups, and are potentially their offspring, to that of unfamiliar juveniles, and whether juveniles could discriminate between familiar adult males and females of their family group (probably their parents) and unfamiliar unrelated adults. We measured tongue flick behavior to study chemosensory responses to the scent of conspecifics. We found that adult female amphisbaenians, but not males, could discriminate between scents of familiar and unfamiliar juveniles. Juvenile amphisbaenians did not discriminate between familiar and unfamiliar adult females, but recognize familiar from unfamiliar males. We discuss our results of parent-offspring recognition according to its potential social function in an ecological fossorial context where visibility is limited and chemosensory kin recognition may contribute to the establishment of stable family groups.

Effect of environmental parameters on squamate reptiles in an urban forest fragment in central Amazonia

The increasing urbanization of the Amazonian biome has promoted the creation of several forest fragments surrounded by an urban matrix, but the relationship of animal assemblages to the urban environment, especially in forest fragments, is poorly known. Here we aimed to 1) determine the composition of the squamate fauna of the largest urban forest fragment from central Amazonia, in the Brazilian city of Manaus, and 2) evaluate the influence of environmental parameters on assemblage diversity. We sampled 10 standardized riparian plots through visual search in six surveys between 2008/09 and 2015, totaling 360 observer-hours. We found 15 species of lacertoids (lizards and amphisbaenians) and seven species of snakes through active search. After considering occasional encounters and search in museum collections, we recorded a total of 24 lacertoid and 22 snake species. Multiple regression models indicated that species richness and abundance of individuals increased with the distance from the edge of the fragment, while other structural parameters of the environment did not affect the assemblage. We conclude that this forest fragment 1) consists of a subset of the regional species pool, and 2) undergoes reduction of species richness and abundance of individuals from the center to the borders. This and additional urban forest fragments should be continually monitored in order to evaluate their long-term role in maintaining the tropical biodiversity. (AU)

Absence of haemoparasite infection in the fossorial amphisbaenian Trogonophis wiegmanni.

Blood parasites such as haemogregarines and haemosporidians have been identified in almost all groups of vertebrates. However, very little is known about biodiversity of these parasites and their effects on some major groups of reptiles such as amphisbaenians, a distinctive group with many morphological and ecological adaptations to fossorial life. Conditions of the fossorial environment might also affect host-parasite relationships. We investigated the presence and the potential prevalence of three genera of haemoparasitic aplicomplexan blood parasites (Hepatozoon, Plasmodium and Haemoproteus) in the amphisbaenian Trogonophis wiegmanni, a fossorial worm lizard species from North West Africa. Blood parasite infection was not detected in T. wiegmanni, both in visual surveys of blood smears and using molecular methods to detect DNA of such parasites in the blood of the potential amphisbaenian hosts. We discuss how conditions of the fossorial environment might affect blood parasitaemias in amphisbaenians as well as in other fossorial reptiles.

The homology of the pelvic elements of Zygaspis quadrifrons (Squamata: Amphisbaenia).

Limb attenuation with element loss has occurred multiple times among the Squamata (lizards, snakes, and amphisbaenians). Although most of the attention has been focused on the appendicular bones, we found that the pelvic rudiments have been studied less thoroughly and recurring disagreement is common among different authors studying the same species. We studied the osteology of the pelvic region of female and male Zygaspis quadrifrons with high-resolution X-ray computed tomography data. We report an osteological landmark (acetabulum) not previously detected in this taxon, the presence of which has repercussions that call for a reconsideration of the primary homology hypothesis for the identity of these bones in amphisbaenians and other squamates. Finally, we observed that the acetabulum and limb rudiments in amphisbaenians (i.e., the stylopodium when present) are situated medial to the pelvic girdle, contrasting with the large majority of tetrapods where these structures are laterally oriented.

An overview of the South American fossil squamates.

The evolution of squamates in South America is the result of the complex geological and paleoclimatic history of this part of the world. The incomplete and episodic fossil record allows us to know only a small part of this evolution. Most Mesozoic squamate remains come from the Patagonian region, but remarkable specimens have also been recovered from Brazil. Both major squamate clades (Iguania and Scleroglossa) are present in the South American Mesozoic. Remains of Mesozoic snakes are common and diverse in Cretaceous deposits, including some of the most primitive terrestrial forms. Paleogene and Neogene squamate remains have been recognized from Argentina, Bolivia, Brazil, Colombia, Ecuador, Peru, and Venezuela. Paleogene lizard record appears to be scarce in comparison to that of the Mesozoic, whereas snakes show an important Paleogene diversity. At least two extant boid snakes appeared during this epoch (Boa and Corallus). The South American Miocene included some extant genera of Iguania, Teiidae, and Boidae but extinct genera were also present. "Colubrids" appeared at the early Miocene, whereas the first viperid is known from the late Miocene. Most of the Paleogene and early Neogene squamate families and genera have been recognized outside their current range of distribution following favorable climatic conditions for ectothermic vertebrates. During the latest Miocene and Pliocene few extant squamate taxa are found to occur outside their present distribution. The earliest amphisbaenian of South America is known from the Pliocene. Most Pleistocene and Holocene squamate remains are assigned to living genera, and some extant species were recognized.