Crotalus Willardi Research Articles

Warm Springs Are Associated with Early Births in Three Montane Rattlesnake Species

A warming climate is correlated with phenological shifts in many taxa. We analyzed data from two long-term field studies of three viviparous viperid snakes to examine correlations between temperature and parturition dates. We studied Rock Rattlesnakes (Crotalus lepidus) and Ridge-Nosed Rattlesnakes (Crotalus willardi) over a 31-yr period and Twin-Spotted Rattlesnakes (Crotalus pricei) over a 23-yr period. On average, a 1°C increase in mean daily maximum temperature during mid-April to June, the probable gestation period, was associated with C. lepidus litters being found 6.0 ± 0.84 days earlier and C. willardi litters being found 5.7 ± 1.79 days earlier. We were more likely to find C. pricei neonates during surveys in late July following warm springs and pregnant females in late July following cool springs. Although earlier parturitions could potentially increase maternal survival and improve lifetime reproductive output, warmer temperatures during embryo development could cause unviability or neonate abnormalities. Neonate survival would probably be negatively affected if births occurred before the onset of the summer monsoon rains. Populations of these species that inhabit the highest elevations of mountain ranges will be unable to shift their distributions to maintain the thermal conditions under which they evolved.

Venom phenotypes of the Rock Rattlesnake (Crotalus lepidus) and the Ridge-nosed Rattlesnake (Crotalus willardi) from México and the United States

Although the Mexican Highlands has the highest diversity of small-bodied rattlesnakes in the world, studies on the species found throughout this region have been relatively scarce. This has led to challenges with examining venom phenotypic characteristics, as well as species misidentifications and misclassifications. In the current study we investigated venom variation among four subspecies of Crotalus lepidus (C. l. klaluberi, C. l. lepidus, C. l. maculosus, C. l. morulus) and four subspecies of C. willardi (C. w. amabilis, C. w. obscurus, C. w. silus, and C. w. willardi) that inhabit regions of southwestern United States and central México. SDS-PAGE patterns show the presence of many of the major compounds found in other rattlesnake venoms, although minor variations in protein banding patterns and intensity are recognizable. Most notably, PI-metalloproteinase (SVMP) bands appear to be very faint to absent in northern C. l. lepidus and C. l. klauberi subspecies, but are fairly prominent in all other C. lepidus and C. willardi subspecies. Enzyme activity assays revealed that C. lepidus subspecies exhibit higher SVMP and thrombin-like activities when compared to C. willardi subspecies. Significant differences between subspecies were also observed for kallikrein-like serine protease, L-amino acid oxidase, and phosphodiesterase activities, although these differences appear to be random and fail to follow a geographical or phylogenetic trend. The same relationship was also observed for fibrinogenolytic and coagulation assays. Toxicity assays conducted on lab mice (Mus musculus), house geckos (Hemidactylus frenatus), and house crickets (Acheta domestica) revealed varying toxicities between subspecies, with C. l klauberi being the most toxic towards mice (LD50 = 1.36 μg/g) and house geckos (LD50 = 0.17 μg/g), and C. w. silus being most toxic to house crickets (LD50 = 1.94 μg/g). These results provide additional evidence that geographical isolation, natural selection, and adaptive evolution in response to diets may be driving forces contributing to population-level variation in venom composition.

Nowhere to Go but Up: Impacts of Climate Change on Demographics of a Short-Range Endemic (Crotalus willardi obscurus) in the Sky-Islands of Southwestern North America.

Biodiversity elements with narrow niches and restricted distributions (i.e., ‘short range endemics,’ SREs) are particularly vulnerable to climate change. The New Mexico Ridge-nosed Rattlesnake (Crotalus willardi obscurus, CWO), an SRE listed under the U.S. Endangered Species Act within three sky islands of southwestern North America, is constrained at low elevation by drought and at high elevation by wildfire. We combined long-term recapture and molecular data with demographic and niche modeling to gauge its climate-driven status, distribution, and projected longevity. The largest population (Animas) is numerically constricted (N = 151), with few breeding adults (Nb = 24) and an elevated inbreeding coefficient (ΔF = 0.77; 100 years). Mean home range (0.07km2) is significantly smaller compared to other North American rattlesnakes, and movements are within, not among sky islands. Demographic values, when gauged against those displayed by other endangered/Red-Listed reptiles [e.g., Loggerhead Sea Turtle ( Caretta caretta )], are either comparable or markedly lower. Survival rate differs significantly between genders (female<male) and life history stages (juvenile<adult) while a steadily declining population trajectory (r = -0.20±0.03) underscores the shallow predicted-time-to-extinction (17.09±2.05 years). Core habitat is receding upwards in elevation and will shift 750km NW under conservative climate estimates. While survival is significantly impacted by wildfire at upper elevations, the extinction vortex is driven by small population demographics, a situation comparable to that of the European Adder (Vipera berus), a conservation icon in southern Sweden. Genetic rescue, a management approach successfully employed in similar situations, is ill advised in this situation due to climate-driven habitat change in the sky islands. CWO is a rare organism in a unique environment, with a conserved niche and a predisposition towards extinction. It is a bellwether for the eventual climate-driven collapse of the Madrean pine-oak ecosystem, one of Earth’s three recognized megadiversity centers.

Prevalence of Salmonella spp. and serogroups found in venomous and nonvenomous snakes maintained in a zoological collection

This study set out to identify Salmonella species and serogroups found in the fecal matter from the snake collection, including venomous snakes, from a local zoo. Snakes are known asymptomatic carriers ofSalmonella spp. Previous studies have shown that Salmonella subspecies arizoniae can cause osteomyelitis in Ridgenose Rattlesnakes (Crotalus willardi). This study examining the carriage rate of serogroups in multiple snake species can help determine the possible spread of clinically significant Salmonella spp. within the collection and possible disease manifestations in both humans and snakes. All fecal samples were collected by professionally trained reptile keepers. Feces were placed in buffered peptone water using aseptic technique. The samples were then enriched using selenite broth and plated for isolation on hektoen enteric agar. Single colonies that tested positive motility, negative indole reaction, and negative for urease were sequenced using 16s ribosomal sequencing techniques. The samples were also serogrouped using a latex agglutination test. A total of thirty‐two samples were taken from twenty‐six species of snakes. Of the samples, 84.38% (27/32) had positive Salmonella colonies. The twenty‐seven positive Salmonella colonies were isolated and sequenced from 22 species of snakes. Serogrouping revealed clinically significant Salmonella serogroups C, A, B, and E or G. Clinically significant Salmonella spp. were found to be prevalent in the venomous and nonvenomous snakes. Polymerase Chain Reaction (PCR) is being conducted to examine the pathogenicity islands from the isolates.

Diet of New Mexico Ridge-nosed Rattlesnake (Crotalus willardi obscurus) in the Sierra San Luis and Sierra Pan Duro, México

Abstract We examined the diet of New Mexico Ridge-nosed Rattlesnakes (Crotalus willardi obscurus) from the Sierra San Luis and the Sierra Pan Duro in the northern Sierra Madre Occidental, Mexico. All snakes included in this study were encountered during August, September, and October in 2003 and 2004. Including recaptures of previously captured individuals, 107 of 199 snakes contained at least one prey item. We examined 103 prey items from 92 of these snakes; some snakes contained multiple prey items. Approximately two-thirds of prey items were ectotherms (54.4% lizards and 13.6% scolopendromorph centipedes); birds (21.4%) and mammals (10.7%) were also taken. The diet of juvenile snakes (n = 32) consisted primarily of lizards (62.5%) and centipedes (25.8%), although large juveniles also consumed mammals (6.3%) and passerine birds (6.3%). Adult snakes (n = 71) fed primarily on lizards (50.7%) and passerine birds (28.2%) but also consumed mammals (12.7%) and centipedes (8.4%). Crotalus willardi in the Sierr...

Rattle Button Loss in Juvenile Ridge-nosed Rattlesnakes (Crotalus willardi): A Novel Mechanism for the Developmental Delay of the Rattle

Although a keratinous rattle structure at the end of the tail is the defining trait of rattlesnakes, there is variation in the ability of rattles to produce sound. In previously reported cases of reduced rattle functionality, near complete loss of sound production occurs in adult snakes that do not retain loose interlocking rattle segments. Here we report for the first time a distinct phenomenon: the delay in development of a functional rattle among neonate and juvenile Ridge-nosed Rattlesnakes (Crotalus willardi) resulting from universal loss of the rattle button, normally the first loose segment retained in functional rattles. Loose segments added during subsequent sheds are retained at rates similar to two other rattlesnake species examined (based on data from over 1,000 wild-caught rattlesnakes) and presumably other rattlesnakes with sound-producing rattles. This pattern of delayed rattle development results in effectively silent cohorts for approximately the first year of life and provides further insight into the ecological context of rattle function and evolution.

Geographic isolation, genetic divergence, and ecological non-exchangeability define ESUs in a threatened sky-island rattlesnake

We utilized nine microsatellite loci and 865 bases from two mtDNA genes to estimate demographic parameters and visualize historic/contemporary connectivity among populations of a sky-island rattlesnake (New Mexico ridge-nosed rattlesnake, Crotalus willardi obscurus). This taxon is listed as threatened under the United States Endangered Species Act (ESA) and is distributed patchily within three borderland mountain ranges [Animas (ANM), Peloncillo (PEL), Sierra San Luis (SSL)] of southeastern Arizona, southwestern New Mexico and north-central México. Molecular data support a hypothesis of northward range expansion from México, with subsequent isolation on sky-islands through vicariant desertification that transformed intervening wooded valleys and low elevation passes into inhospitable habitat. Historic and recent movements have been within rather than among mountains. Although populations are linked via ancestral polymorphism, they do not represent a single mtDNA gene pool. All are genetically bottlenecked, with the Peloncillo reflecting deepest/sharpest declines and fewest captures per unit effort. Most recent population declines occurred ∼4 kybp (thousands of years before present). Thus, population reductions are historic and environmental rather than contemporary and anthropogenic. Our data demonstrate that PEL is ecologically non-exchangable with other sky-island populations, and thus comprises one ‘evolutionary significant unit’ (ESU), while SSL and ANM comprise ‘management units’ (MUs) within a second ESU. All three meet legal criteria for recognition as ‘distinct population segments’ (DPS) under the ESA.

SALMONELLA SURVEILLANCE IN A COLLECTION OF RATTLESNAKES (CROTALUS SPP)

Over the past 15 yr, Salmonella enterica ssp. arizonae (IIIa) 56:z4,z23:- has repeatedly been isolated from individual Crotalus willardi rattlesnakes with progressively debilitating osteomyelitis at the Knoxville Zoological Gardens. In April 2004, the serotype was linked with a fatal case of septicemia in another Crotalus species in this collection. Although the association of IIIa 56:z4,z23:- with disease in this colony of C. willardi is well established, prior disease or isolation of this serotype outside of the C. willardi colony had not been documented previously, and the serotype's distribution throughout the remainder of the Crotalus collection had yet to be determined. Forty-one fecal samples were obtained from each individual (n = 36) or exhibit group (n = 5) of crotalid snakes, representing nine species, housed at the zoo. Salmonella spp. were isolated from every sample, with 21 different serotypes. The 21 serotypes were distributed among S. enterica ssp. I (24%), IIIa (9%), and IIIb (67%). Although not recovered in the primary study, S. arizonae 56:z4,z23:- was recovered from additional samples taken from two C. willardi willardi. Although the overall recovery rate of this serotype from feces has been low, it seems that its distribution among the Crotalus collection at Knoxville Zoological Gardens remains largely restricted to the C. willardi species.

SPINAL CORD GLIOMA IN A RIDGE-NOSED RATTLESNAKE (CROTALUS WILLARDI)

An 11-yr-old, female Arizona ridge-nosed rattlesnake (Crotalus willardi) had a 1-yr history of retained egg masses and decreased mobility in the caudal two-thirds of the body. The snake was euthanized when it became unable to right itself. At necropsy, the caudal portion of the spinal cord was found to be enlarged, soft, and translucent pale gray. Microscopically, the caudal portion of the spinal cord was segmentally replaced by a neoplastic mass composed of cells resembling glia (oligodendrocytes and astrocytes). Immunohistochemistry for glial fibrillary acidic protein was positive in the astrocytelike neoplastic cells. The gross, microscopic, and immunohistochemical findings were consistent with a diagnosis of spinal cord glioma. This is the first report of a central nervous system tumor in a reptile.

Comparison of phenotypic traits and genetic relatedness of Salmonella enterica subspecies arizonae isolates from a colony of ridgenose rattlesnakes with osteomyelitis.

Reptiles are well-known sources of human Salmonella infections; however, little is known about the ability of Salmonella to cause disease in reptiles. Thirty-seven isolates of Salmonella enterica subspecies arizonae (S. arizonae) were obtained from retrospective and prospective studies of a closed colony of ridgenose rattlesnakes (Crotalus willardi) with osteomyelitis. All isolates (N = 7) from bone lesions were of a single serotype, 56:z4,z23, and this serotype was found on only 1 occasion among 8 other serotypes isolated from 21 cloacal and intestinal samples. The remainder (N = 7) of serotype 56:z4,z23 isolates were from other extraintestinal sites, including liver, ovary, blood, and testis. S. arizonae isolates were susceptible to most antimicrobials, and plasmid profiles did not correlate with serotype or antimicrobial resistance. Isolates of the 56:z4,z23 serotype (N = 14) formed a tight cluster with 95% similarity by XbaI macrorestriction analysis. Individual isolates of serotypes, 56:z4,z23, 38:(k)-z35, and 48:i-z invaded HeLa cells but an isolate of serotype 50:r-z did not. The same individual isolates of serotype 56:z4,z23 and 48:i-z also invaded viper heart cells. The Salmonella InvA gene was detected by polymerase chain reaction (PCR) in all S. arizonae serotypes tested, including 5 serotype 56:z4,z23 isolates and individual isolates of serotypes 48:i-z and 50:r-z. A source or possible explanation for increased virulence of S. arizonae serotype 56:z4,z23 in this unique host has not been found.

Osteomyelitis associated with Salmonella enterica SS arizonae in a colony of ridgenose rattlesnakes (Crotalus willardi).

The identification of three Arizona ridgenose rattlesnakes (Crotalus willardi) with Salmonella arizonae-associated osteomyelitis led to a 5-yr prospective study of radiographic signs and Salmonella intestinal carriage rates in a 19-member colony of this rattlesnake species. Ventrodorsal radiographs were performed and cloacal swabs were cultured for Salmonella spp. annually. Ten snakes survived the 5-yr period, with six of them remaining free of bony lesions. Three snakes that had no bony lesions in 1995 developed radiographic signs of osteomyelitis during the study. Six snakes with bony lesions at the beginning of the study died or were euthanatized due to osteomyelitis during the study. The radiographic signs of osteomyelitis were progressive for five snakes that were serially radiographed. Only one snake with radiographic signs of osteomyelitis at the beginning of the study was still alive at the end of the study, and this animal's bony lesions were more extensive at the end. Thirty-nine intestinal S. arizonae isolates, representing 13 serotypes, were obtained from the 19 snakes. Salmonella arizonae serotype 56:Z4,Z23 was isolated only once from a cloacal culture, from a snake that had no radiographic bone lesions. Twelve extraintestinal Salmonella isolates, representing two serotypes, were isolated from six snakes. All extraintestinal isolates except one were of S. arizonae serotype 56:Z4,Z23, and all isolates from bone were of this serotype. One snake with characteristic bone lesions died, and Providencia rettgeri was cultured from each of the tissues cultured, whereas no Salmonella spp. were isolated from this snake. Salmonella arizonae serotype 56:Z4,Z23 [corrected] appears to have a tropism for bone and other extraintestinal sites in C. willardi and may cause a progressive, ultimately fatal disease in this species.

Isolation and characterization of microsatellite loci from a threatened rattlesnake (New Mexico Ridge‐nosed Rattlesnake, Crotalus willardi obscurus)

AbstractSix novel microsatellite loci are identified from genomic DNA of the threatened New Mexico Ridge‐nosed Rattlesnake (Crotalus willardi obscurus). Data from the Animas Mountains (New Mexico) population demonstrate these loci: (i) are highly variable with 5–24 alleles per locus, expected heterozygosities between 0.35 and 0.92, and observed heterozygosities between 0.32 and 0.91; (ii) are sufficiently variable for assigning parentage with total exclusionary power for the first parent of 0.96, and 0.99 for the second parent; and (iii) amplify similar size fragments in other rattlesnakes (C. atrox, C. lutosus, C. scutulatus, and C. tigris).

Observations of Predation on Crotalus willardi obscurus in the Animas Mountains, New Mexico

course of an ongoing mark-recapture investigation of the ecology of a montane snake community in the Animas Mountains, Hidalgo Co., New Mexico. A male C. w. obscurus (188 g, 580 mm snout-vent length [SVL]) first captured 7 October 1998 was recaptured 2 June 1999. A miniature radio-transmitter was then surgically implanted in the body cavity and the specimen was released 3 days later at its capture location at an elevation of 2,240 m. The snake was located daily and moved an average of 23.6 m each day (SE = 7.0, range = 0-78.4) from 7 to 20 June 1999. From 14 to 20 June the snake contained an exceptionally large prey bulge. Post-prandial thermophily may have increased exposure to predators and compromised agility may have increased vulnerability (Garland and Arnold, 1983; Ford and Shuttlesworth, 1986). On 21 June at 1600 h a portion of the snake (University of New Mexico, Museum of Southwest Biology, Division of Herpetology, MSB 61426) containing the radio-transmitter was found 14 m from the snake's location the

Reproduction in Northern Populations of the Ridgenose Rattlesnake,Crotalus willardi(Serpentes: Viperidae)

Abstract We describe the reproductive biology of northern populations of Crotalus willardi using data gathered from four long-term field studies, histological examination of museum specimens, and literature records. Spermiogenesis occurs summer to early autumn. All male C. willardi examined contained sperm in the vas deferens (June–September) and had enlarged kidney sexual segments (June–October). Parturition occurs from late July through August (n = 17). Postpartum females appear to remain reproductively inactive prior to hibernation. Secondary yolk deposition (vitellogenesis) commences in the late spring or early summer, one or more years after parturition. Ovulation and fertilization probably occur early in the spring, followed by 4–5 months gestation. Copulation occurs in midsummer to early fall (n = 10). Repeated observations of marked females over several years, proportion of adult gravid females (60% Crotalus willardi obscurus, 40% Crotalus willardi willardi, 51% pooled), observations on captive an...

A New Subspecies of the Ridged-Nosed Rattlesnake, Crotalus willardi, from Chihuahua, Mexico

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The subspecies of the ridge-nosed rattlesnake, Crotalus willardi

The subspecies of the ridge-nosed rattlesnake, Crotalus willardi

Description of a little-known rattlesnake, Crotalus willardi, from Arizona

Description of a little-known rattlesnake, Crotalus willardi, from Arizona