Distribution,abundance, and habitat use of introduced <Emphasis Type="Italic">Boa constrictor</Emphasis> threatening the native biota of Cozumel Island,Mexico

Species introductions are among the most pervasive types of disturbance, seriously affecting island biota and ecosystem dynamics. The management of introduced generalist species, which may live in a wide range of environmental conditions, can be particularly difficult and is a major challenge for the conservation of native insular species. Boa constrictor was introduced onto Cozumel Island, Mexico, in 1971. The introduction of this generalist predator has affected negatively the native species (many of them endemic to the island) on which the boa feed. It is important to determine temporal variation in boa abundance, the areas of the island in which boas live, and the vegetation types they use in order to develop management strategies to reduce boa pressure on the native biota. We used nocturnal road transect sampling and occasional boa encounters during field work, to estimate boa distribution, abundance and habitat use, taking into account its spatiotemporal patterns on Cozumel Island. This study confirms that Boa constrictor is well established, widespread, and abundant on the island. Our results show that boas are distributed throughout Cozumel, in all vegetation types and geographical regions. Overall, there were 0.11 ± 0.03 boa/10 km road transect. There were no significant spatiotemporal differences in boa activity (time of day) and abundance (monthly, seasonally, by vegetation types or regions of the island). According to the habitat use analysis, there were, however, fewer boas than expected in the subdeciduous tropical forest we sampled and in the central-northern region of the island, which coincide with areas inhabited by humans. There were more boas in areas uninhabited by humans, and there was a tendency towards a greater proportion of dead boas in inhabited areas and live boas in uninhabited areas. Cozumel boas are habitat generalists, which are affected by human induced mortality in inhabited areas. There is a vast area uninhabited by humans, with natural vegetation, on the island where boas have suitable habitats available for their continuous existence on Cozumel. This situation, and the adaptability of the boa, makes the control or eradication of this introduced species a critical conservation challenge.     

DID EGG‐LAYING BOAS BREAK DOLLO'S LAW? PHYLOGENETIC EVIDENCE FOR REVERSAL TO OVIPARITY IN SAND BOAS (ERYX: BOIDAE)

Re-evolution of lost complex morphological characters has been proposed for several characters, including insect wings, limbs, eyes in snakes, and digits in lizards, among others. There has also been much interest in whether the transition from oviparity to viviparity is reversible, particularly in squamate reptiles where the transition to viviparity has occurred more times than in any other lineage. Here, we present a phylogenetic analysis of boid snakes based on a concatenated multigene study of all genera of erycines, New and Old World boines, plus other groups thought to be closely related with boines such as monotypic species Calabaria and Casarea . We reconstruct ancestral parity mode on this phylogeny and present statistical evidence that oviparity reevolved in a species of Old World sand boa in the genus Eryx nearly 60 million years after the initial boid transition to viviparity. Remarkably, like other viviparous boas hatchlings of oviparous Eryx lack an egg-tooth providing independent evidence that oviparity is a derived state in these species.     

Adaptive maternal cannibalism in snakes (Epicrates cenchria maurus, Boidae)

In many animal species, mothers that produce stillborn offspring or undeveloped ova immediately ingest them. This cannibalism has been interpreted in two ways: (1) as a form of parental care (to prevent disease spreading to healthy littermates, and eliminate predator-attracting scent cues); or (2) to recycle otherwise wasted energy, thus facilitating maternal recovery. Our experimental study on captive Colombian rainbow boas ( Epicrates cenchria maurus ) provides the first quantitative support for this latter hypothesis. We show that by eating their non-viable offspring and undeveloped eggs, female boas can rapidly recycle a significant component of their otherwise wasted reproductive investment. Female boas that ingested non-viable progeny equivalent to half their litter mass exhibited rapid recovery of dorsal musculature and hence were able to constrict prey items more forcefully than were unfed females when tested 2 weeks after parturition. The consequent enhancement of constricting ability may influence maternal survival and foraging success. Thus, maternal cannibalism may be an effective tactic to avoid wasting reproductive resources, and to shorten the period required for recovery from pregnancy.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 767–774.     

Predicted population trends for Cozumel Curassows (Crax rubra griscomi): empirical evidence and predictive models in the face of climate change

ABSTRACT We assessed the current conservation status and population trends of Cozumel Curassows (Crax rubra griscomi), a critically endangered and endemic cracid of Cozumel Island, Mexico. Distance sampling was used to estimate the population size in 2005 and compare it with a previous estimate in 1995. Population viability analysis (PVA) was used to model population trends, considering ecological and environmental conditions prevailing in 1995 and 2005. Additional PVA models were constructed using different hypothetical scenarios to assess the effects of particular factors and management strategies on population trends. We estimated a population size of 372 ± 155 curassows in the island's tropical semideciduous forest, before two hurricanes hit Cozumel Island in 2005. PVA modeling predicted a steep decline in population size in the ensuing decades as a result of an increased frequency and intensity of hurricanes related to global climate change, and an observed female bias in the sex ratio likely caused by a higher mortality rate for adult males. We recommend urgent management actions for the long‐term conservation of Cozumel Curassows, including a ban on hunting, eradication of the feral fauna, particularly dogs, and implementation of a captive‐breeding program to supplement the wild population.     

The status of dwarf carnivores on Cozumel Island, Mexico

Cozumel Island in the Mexican Caribbean is inhabited by four carnivores, of which two, the Cozumel coati Nasua nelsoni and pygmy raccoon Procyon pygmaeus, are endemic species. The taxonomic status of a third carnivore, a dwarf gray fox Urocyon cinereoargenteus, is undetermined, but may deserve subspecific or species-level recognition. The fourth species, the kinkajou (Potos flavus), may be a recent introduction. We review the status of these carnivores, report our field observations and results of line transect and trapping efforts, discuss current threats to these taxa, and make recommendations for their conservation. A population density of 0.43 ± 0.27 coatis/km², and a total island population size of 150 ± 95 individuals, was estimated from 386 km of line transects in 1994–1995. Intensive trapping efforts (1479 trap-nights) in 2001 at multiple localities were unsuccessful. Pygmy raccoons were observed in the mangrove and coastal wetland areas of the island and in 2001 we captured 11 individuals with the same sampling efforts as for coatis (8.8 raccoons/1000 trap-nights). The gray fox is also apparently very rare on the island. While a few observations of the animals have been made (1984, 1994 and 2001), no animals were seen along transects and none were trapped. The primary threats to the persistence of these taxa include introduced congeners, introduced predators, parasite and disease spill-over from exotic animals, habitat fragmentation, hunting and collection as pets, and hurricanes. We suggest that the Cozumel coati, pygmy raccoon, and the Cozumel population of the gray fox be considered as Critically Endangered according to the IUCN classification system. Current conservation actions focusing on Cozumel carnivores are extremely limited. We recommend eradication of introduced species, maintenance of habitat connectivity, ex situ conservation programs, explicit public policies on land-use and sustainable development, public awareness campaigns, and continuous scientific research and monitoring.     

Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support

Four New World genera of dwarf boas (Exiliboa, Trachyboa, Tropidophis, and Ungaliophis) have been placed by many systematists in a single group (traditionally called Tropidophiidae). However, the monophyly of this group has been questioned in several studies. Moreover, the overall relationships among basal snake lineages, including the placement of the dwarf boas, are poorly understood. We obtained mtDNA sequence data for 12S, 16S, and intervening tRNA-val genes from 23 species of snakes representing most major snake lineages, including all four genera of New World dwarf boas. We then examined the phylogenetic position of these species by estimating the phylogeny of the basal snakes. Our phylogenetic analysis suggests that New World dwarf boas are not monophyletic. Instead, we find Exiliboa and Ungaliophis to be most closely related to sand boas (Erycinae), boas (Boinae), and advanced snakes (Caenophidea), whereas Tropidophis and Trachyboa form an independent clade that separated relatively early in snake radiation. Our estimate of snake phylogeny differs significantly in other ways from some previous estimates of snake phylogeny. For instance, pythons do not cluster with boas and sand boas, but instead show a strong relationship with Loxocemus and Xenopeltis. Additionally, uropeltids cluster strongly with Cylindrophis, and together are embedded in what has previously been considered the macrostomatan radiation. These relationships are supported by both bootstrapping (parametric and nonparametric approaches) and Bayesian analysis, although Bayesian support values are consistently higher than those obtained from nonparametric bootstrapping. Simulations show that Bayesian support values represent much better estimates of phylogenetic accuracy than do nonparametric bootstrap support values, at least under the conditions of our study.     

Foraging Behavior in the Arboreal Boid Corallus grenadensis

Corallus grenadensis is an arboreal boa endemic to the Grenada Bank. Thirty-five encounters with boas resulted in 17.65 hours of observations, including 6.3 hours of video-tape (which included two acts of predation). Boas under 100 cm are largely active foragers that move slowly through bushes and trees and tongue-flick leaf and branch surfaces apparently seeking chemosensory evidence of nocturnally quiescent lizard (Anolis) prey. Significantly more search time was directed to branches below the snake rather than to either the branches supporting the snake or to those above the snake, and tongue-flick rates were significantly higher for moving snakes than for those that were stationary. Smaller snakes prey on nocturnally quiescent lizards and they spent more time moving than did large snakes that feed on nocturnally active rodents and often employ an ambush foraging strategy. Once visual and, presumably, thermal information was received from a sleeping anole, C. grenadensis adopted a lengthy stalking process devoid of tongue-flicks. Snakes approached inactive lizards from adjacent branches with great stealth, moving at a rate of about 1 cm/min. The strike was made from close range (within 3 cm), and the prey was never released once contact was made. We conclude that, if chemosensory cues successfully lead a treeboa to a visual encounter with a sleeping lizard, subsequent behavior ensures a high rate of predation success.     

New insights on the geographical origins of the Caribbean raccoons

The introduction of species outside their natural range is one of the major threats to biodiversity and has often been identified as a menace to agricultural production and human health. The raccoon is recognized as a globally invasive species. However, several populations in the Caribbean were long considered native and endemic species. Although previous genetic studies have shown that raccoons from the islands of the West Indies belong to the northern raccoon Procyon lotor, the history and origin of these introductions remain poorly known. In this study, we investigated the geographical origin of Caribbean raccoon populations using newly available molecular genetic data. We used haplotype network analyses of two mitochondrial markers, Cytochrome b and Control Region, with new sequences and those from GenBank. We also specifically investigated the origin of the endangered endemic Cozumel raccoon, Procyon pygmaeus, by re-analyzing data. Our results confirmed that all Caribbean raccoon populations belong to the northern raccoon. Bahamian populations originated from two different sources in Florida, and the Lesser Antilles raccoons seem to originate from northern regions of the native range. In addition, our results question the taxonomic status of the Cozumel raccoon, as currently available genetic data support a conspecific status with the northern raccoon. These results have important implications in the context of conservation and ecosystem management. Identifying origins of introduced populations and understanding the history of their introductions will facilitate studies on the impact of the raccoon on insular ecosystems.     

Genetic diversity in the US ex situ populations of the endangered Puerto Rican Boa,Chilabothrus inornatus

The Puerto Rican Boa (Chilabothrus inornatus) was placed on the US Endangered Species List in 1970. Progress has been made since to clarify the recovery status of this species, though the design of a new recovery plan must include information regarding genetic variation within and among populations of this species. While measures of genetic diversity in wild populations of this species are finally becoming available, relative genetic diversity represented in ex situ populations is unknown, which hampers efforts to develop an ex situ species management plan. Here, we provide an analysis of genetic diversity in US public and private collections (zoos and breeders) using mitochondrial sequence data and five highly polymorphic nuclear microsatellite loci. We analyzed 50 boas from the US ex situ population and determined overall genetic diversity and relatedness among these individuals. We then compared these data to mitochondrial and microsatellite data obtained from 176 individuals from wild populations across the native range of the species. We found little inbreeding and a large amount of retained genetic diversity in the US ex situ population of C. inornatus relative to wild populations. Genetic diversity in the ex situ population is similar to that found in wild populations. Ours is only the second explicit attempt to characterize genetic diversity at the molecular level in ex situ populations of boid snakes. We anticipate that these results will inform current breeding strategies as well as offer additional information that will facilitate the continuation of ex situ conservation breeding or management in boas.     

Pulmonary defense mechanisms in Boa constrictor

We studied aerosol deposition and the response to inhaled particles and irritants in lungs of Boa constrictor. Snakes which breathed submicrometric particles radiolabeled with 99mTc retained 41.4 +/- 9.9% of the aerosol in the trachea, 42.5 +/- 8.8% in the anterior faveolar regions, and 8.7 +/- 4.1% in the posterior saccular regions of the lungs. Low activity recovered in the gastrointestinal tract over a 5-h period following aerosol exposure indicated slow clearance of inhaled particles. In contrast to mammalian lungs, there are no macrophages resident on the surface of boa lungs, and uningested particles persist for up to 4 days without being phagocytized. Particles and irritant stimuli (Fe2O3, endotoxin, and N-formylmethionylphenylalanine) elicited only eosinophilic granulocytes that were not phagocytic. The numbers of these cells peaked at 24 h following exposure and declined gradually over the next 7 days. Lavage fluid from stimulated snake lungs contained many large lamellar figures continuous with tubular myelin, a form of surfactant. Very little of this material was recovered from control lungs. Response to inhaled particles and lung injury in boas increased surfactant release, elicited eosinophilic granulocytes, but did not recruit phagocytic mononuclear cells.     

High genetic structure of the Cozumel Harvest mice,a critically endangered island endemic: conservation implications

We assessed the genetic structure and diversity of Reithrodontomys spectabilis, a critically endangered, endemic rodent from Cozumel Island, México. A total of 90 individuals were trapped from September 2001 to January 2005. Microsatellite data analysis revealed high genetic diversity values: a total of 113 alleles (average 12.5 per locus), H _o  = 0.78, H _e  = 0.80. These high values can be related to Cozumel’s size (478 km²) and extensive native vegetation cover, factors that could be promoting a suitable population size, high heterozygosity and the persistence of rare alleles in the species, as well as some long-term movement of individuals between sampling localities. A strong genetic structure was also observed, with at least four genetic groups, associated with a pattern of isolation by distance. We found a strong allelic and genetic differentiation shown between localities, with negligible recent gene flow and low inbreeding coefficients. The species life history and ecological characteristics—being nocturnal, semi-terrestrial, a good tree climber, having lunar phobia and significant edge effect—are likely affecting its genetic structure and differentiation. The high genetic diversity and population structure award R. spectabilis a significant conservation value. Our results can serve as a basis for future research and conservation of the species, particularly considering the problems the island is facing from habitat perturbation, urbanization and introduction of exotic species. In view of the structure and genetic variability observed, it is essential to establish and reinforce protected areas and management programs for the conservation of the endemic and endangered Cozumel Harvest mice.     

Population structure of an endemic vulnerable species, the Jamaican boa (Epicrates subflavus)

The Jamaican boa (Epicrates subflavus; also called Yellow boa) is an endemic species whose natural populations greatly and constantly declined since the late 19th century, mainly because of predation by introduced species, human persecution, and habitat destruction. In-situ conservation of the Jamaican boa is seriously hindered by the lack of information on demographic and ecological parameters as well as by a poor understanding of the population structure and species distribution in the wild. Here, using nine nuclear microsatellite loci and a fragment of the mitochondrial cytochrome b gene from 87 wild-born individuals, we present the first molecular genetic analyses focusing on the diversity and structure of the natural populations of the Jamaican boa. A model-based clustering analysis of multilocus microsatellite genotypes identifies three groups that are also significantly differentiated on the basis of F-statistics. Similarly, haplotypic network reconstruction methods applied on the cytochrome b haplotypes isolated here identify two well-differentiated haplogroups separated by four to six fixed mutations. Bayesian and metaGA analyses of the mitochondrial data set combined with sequences from other Boidae species indicate that rooting of the haplotypic network occurs most likely between the two defined haplogroups. Both analyses (based on nuclear and mitochondrial markers) underline an Eastern vs. (Western + Central) pattern of differentiation in agreement with geological data and patterns of differentiation uncovered in other vertebrate and invertebrate Jamaican species. Our results provide important insights for improving management of ex-situ captive populations and for guiding the development of proper in-situ species survival and habitat management plans for this spectacular, yet poorly known and vulnerable, snake.     

Immunohistochemical Detection of a Unique Protein within Cells of Snakes Having Inclusion Body Disease,a World-Wide Disease Seen in Members of the Families Boidae and Pythonidae

Inclusion body disease (IBD) is a worldwide disease in captive boa constrictors (boa constrictor) and occasionally in other snakes of the families Boidae and Pythonidae. The exact causative agent(s) and pathogenesis are not yet fully understood. Currently, diagnosis of IBD is based on the light microscopic identification of eosinophilic intracytoplasmic inclusion bodies in hematoxylin and eosin stained tissues or blood smears. An antigenically unique 68 KDa protein was identified within the IBD inclusion bodies, called IBD protein. A validated immuno-based ante-mortem diagnostic test is needed for screening snakes that are at risk of having IBD. In this study, despite difficulties in solubilizing semi-purified inclusion bodies, utilizing hybridoma technology a mouse anti-IBD protein monoclonal antibody (MAB) was produced. The antigenic specificity of the antibody was confirmed and validated by western blots, enzyme-linked immunosorbent assay, immuno-transmission electron microscopy, and immunohistochemical staining. Paraffin embedded tissues of IBD positive and negative boa constrictors (n=94) collected from 1990 to 2011 were tested with immunohistochemical staining. In boa constrictors, the anti-IBDP MAB had a sensitivity of 83% and specificity of 100% in detecting IBD. The antibody also cross-reacted with IBD inclusion bodies in carpet pythons (Morelia spilota) and a ball python (python regius). This validated antibody can serve as a tool for the development of ante-mortem immunodiagnostic tests for IBD.     

ZW,XY, and yet ZW: Sex chromosome evolution in snakes even more complicated

Snakes are historically important in the formulation of several central concepts on the evolution of sex chromosomes. For over 50 years, it was believed that all snakes shared the same ZZ/ZW sex chromosomes, which are homomorphic and poorly differentiated in “basal” snakes such as pythons and boas, while heteromorphic and well differentiated in “advanced” (caenophidian) snakes. Recent molecular studies revealed that differentiated sex chromosomes are indeed shared among all families of caenophidian snakes, but that boas and pythons evolved likely independently male heterogamety (XX/XY sex chromosomes). The historical report of heteromorphic ZZ/ZW sex chromosomes in a boid snake was previously regarded as ambiguous. In the current study, we document heteromorphic ZZ/ZW sex chromosomes in a boid snake. A comparative approach suggests that these heteromorphic sex chromosomes evolved very recently and that they are poorly differentiated at the sequence level. Interestingly, two snake lineages with confirmed male heterogamety possess homomorphic sex chromosomes, but heteromorphic sex chromosomes are present in both snake lineages with female heterogamety. We point out that this phenomenon is more common across squamates. The presence of female heterogamety in non‐caenophidian snakes indicates that the evolution of sex chromosomes in this lineage is much more complex than previously thought, making snakes an even better model system for the evolution of sex chromosomes.     

Trying to collapse a population for conservation: commercial trade of a marine invasive species by artisanal fishers

Implementing new and effective control strategies to reduce populations of invasive species is needed to offset their negative impacts worldwide. The spread of Indo-Pacific lionfish (Pterois sp.) through much of the western Atlantic has been one of the most publicized marine invasions globally, and is considered a major biodiversity threat whose longer-term impacts are still uncertain. Marine managers have explored several strategies to control lionfish, such as fishing tournaments (derbies) and commercial fisheries. Commercial fisheries for invasive species are controversial because they could create perverse incentives to maintain these populations, and they have never been demonstrated to successfully control target populations. We analyzed the development and impacts of an opportunistic fishing operation aimed at commercializing invasive lionfish in the Mexican Caribbean. We examined official lionfish landings and compared them to catches from lionfish derbies and lionfish densities from locations in the state of Quintana Roo, Mexico. We found that commercial fishers, particularly from one fishing cooperative on Cozumel Island, were effective at catching lionfish, with landings peaking at 20,000 individuals in 2014. This number is comparable to the number of lionfish caught in derbies across the entire Caribbean in the same year. Ecological survey data suggest a?~?60% reduction in lionfish density on Cozumel reefs over two years (2013–2015), matching the peak landings in the lionfish fishing operation. However, the fishery’s apparent success as a control tool during the time window analyzed seemed to trigger its own demise: a decline in landings was followed by evaporating market interest and loss of economic viability. If fisheries are to be established and used as management strategies to control future invasions, managers must develop strategic collaboration plans with commercial fishing partners.

     

Physiological and behavioral control of heating and cooling rates in rubber boas, Charina bottae

1. We examined the ability of rubber boas (Charina bottae) to physiologically and behaviorally control their heating and cooling rates between 5 and 35 °C with constrained and unconstrained postural treatments.     

Pythons in the Eocene of Europe reveal a much older divergence of the group in sympatry with boas

Extant large constrictors, pythons and boas, have a wholly allopatric distribution that has been interpreted largely in terms of vicariance in Gondwana. Here, we describe a stem pythonid based on complete skeletons from the early-middle Eocene of Messel, Germany. The new species is close in age to the divergence of Pythonidae from North American Loxocemus and corroborates a Laurasian origin and dispersal of pythons. Remarkably, it existed in sympatry with the stem boid Eoconstrictor. These occurrences demonstrate that neither dispersal limitation nor strong competitive interactions were decisive in structuring biogeographic patterns early in the history of large, hyper-macrostomatan constrictors and exemplify the synergy between phylogenomic and palaeontological approaches in reconstructing past distributions.     

Parallel selective pressures drive convergent diversification of phenotypes in pythons and boas

Pythons and boas are globally distributed and distantly related radiations with remarkable phenotypic and ecological diversity. We tested whether pythons, boas and their relatives have evolved convergent phenotypes when they display similar ecology. We collected geometric morphometric data on head shape for 1073 specimens representing over 80% of species. We show that these two groups display strong and widespread convergence when they occupy equivalent ecological niches and that the history of phenotypic evolution strongly matches the history of ecological diversification, suggesting that both processes are strongly coupled. These results are consistent with replicated adaptive radiation in both groups. We argue that strong selective pressures related to habitat‐use have driven this convergence. Pythons and boas provide a new model system for the study of macro‐evolutionary patterns of morphological and ecological evolution and they do so at a deeper level of divergence and global scale than any well‐established adaptive radiation model systems.