Nerodia Fasciata Research Articles

Morphology and putative function of the colon and cloaca of marine and freshwater snakes

Among tetrapods, evidence for postrenal modification of the urine by the distal digestive tract (including the colon and cloaca) is highly variable. Birds and bladderless reptiles are of interest because the colon and cloaca represent the only sites from which water and ions can be reclaimed from the urine secreted by the kidney. For animals occupying desiccating environments (e.g., deserts and marine environments), postrenal modification of the urine may directly contribute to the maintenance of hypo-osmotic body fluids. We compared the morphology and distribution of key proteins in the colon, cloaca, and urogenital ducts of watersnakes from marine (Nerodia clarkii clarkii) and freshwater (Nerodia fasciata) habitats. Specifically, we examined the epithelia of each tissue for evidence of mucus production by examining the distribution of mucopolysaccharides, and for evidence of water/ion regulation by examining the distribution of Na(+) /K(+) -ATPase (NKA), Na(+) /K(+) /Cl(-) cotransporter (NKCC), and aquaporin 3 (AQP3). NKCC localized to the basolateral epithelium of the colon, urodeal sphincter, and proctodeum, consistent with a role in secretion of Na(+), Cl(-) , and K(+) from the tissue, but NKA was not detected in the colon or any compartment of the cloaca. Interestingly, NKA was detected in the basolateral epithelium of the ureters, suggesting the urothelium may play a role in active ion transport. AQP3 was detected in the ureters and coprodeal complex, consistent with a role in urinary and fecal dehydration or, potentially, in the production of the watery component of the mucus secreted by the coprodeal complex. Since no differences in general cloacal morphology, production of mucus, or the distribution of ion transporters/water channels were detected between the two species, cloacal osmoregulation may either be regulated by proteins not examined in this study or may not be responsible for the differential success of N. c. clarkii and N. fasciata in marine habitats.

Melanophoromas and Iridophoromas in Reptiles

Chromatophoromas are tumours of pigment-producing cells of the skin and are rarely reported in reptiles. These tumours are subclassified on the basis of the type of pigment. The present study characterizes chromatophoromas arising in 26 reptiles, including six snakes, 19 lizards and a tortoise. These include the first reports of melanophoromas in a yellow anaconda (Eunectes notaeus), pigmy rattlesnake (Sistrurus spp.), southern water snake (Nerodia fasciata), veiled chameleon (Chamaeleo calyptratus) and leopard gecko (Eublepharis macularius); the first reports of benign iridophoromas in a savannah monitor (Varanus exanthematicus), veiled chameleon and bearded dragon (Pogona vitticeps); and the first description of a malignant iridophoroma in a bearded dragon. Additionally, in three bearded dragons a 'mucinous' type of melanophoroma is described for the first time. Chromatophoromas generally arose from the skin of the body and head and ranged in size from 0.2 to 2.0cm in diameter. In six cases the animals were humanely destroyed immediately after diagnosis. Three further animals were humanely destroyed following recurrence of their tumour. Six of these nine reptiles had visceral metastases. Grossly, melanophoromas (n=20) were grey or black, while iridophoromas (n=6) were white in colour. Microscopically, most of the tumours were composed of spindle cells with varying pigmentation and 0-2 mitoses per 10 high power fields. Six of the 20 melanophoromas were classified as malignant due to the presence of intravascular tumour cells, visceral metastases, high pleomorphism and/or mitotic figures. Five of the six iridophoromas were classified as benign and the one malignant tumour was defined by the presence of intravascular tumour cells and visceral metastases. Immunohistochemically, melan A and S100 were coexpressed by all of the chromatophoromas.

Renal responses to salinity change in snakes with and without salt glands

To understand renal responses to salinity change in aquatic reptiles, we examined the structure and function of the kidney in three species of snake: a marine species with a salt gland (Laticauda semifasciata), a marine species without a salt gland (Nerodia clarkii clarkii) and a freshwater species without a salt gland (Nerodia fasciata). Both marine species maintained relatively constant plasma ions, even after acclimation to saltwater. By contrast, both plasma Cl(-) and mortality increased with salinity in the freshwater species. To investigate putative renal ion regulatory mechanisms, we examined the distribution and abundance of Na(+)/K(+)-ATPase (NKA) and the Na(+)/K(+)/2Cl(-) cotransporter (NKCC2). In all species, NKA localized to the basolateral membranes of the distal tubule and the connecting segments and collecting ducts only; there was no effect of salinity on the distribution of NKA or on the abundance of NKA mRNA in any species. NKCC2 protein was undetectable in the kidney of any of the species and there was no effect of salinity on NKCC2 mRNA abundance. We also examined the distribution and abundance of aquaporin 3 (AQP3) in the kidney of these species; although putative AQP3 localized to the basolateral membranes of the connecting segments and collecting ducts of all three species, there was no effect of salinity on the localization of the protein or the abundance of the transcript. Interestingly, we found very few differences across species, suggesting that the snake kidney may play a trivial role in limiting habitat use.

Prey morphology constrains the feeding ecology of an aquatic generalist predator

Resource availability and accessibility are primary factors guiding the distribution and abundance of organisms. For generalists, prey availability reflects both prey abundance and differences in quality among prey taxa. Although some aspects of prey quality, such as nutritional composition, are well studied, our understanding of how prey morphology contributes to overall prey quality is limited. Because snakes cannot reduce prey size by mastication, many aspects of their feeding ecology (e.g., maximum prey size, feeding performance, and the degree of postprandial locomotor impairment) may be affected by prey shape. We conducted a uniquely comprehensive comparison of prey quality for a generalist species, the banded watersnake (Nerodia fasciata), using prey that were similar in mass and presumably similar in nutritional composition but different in shape and habitat association. Specifically, we compared nutritional composition and shape of paedomorphic salamanders (Ambystoma talpoideum) and sunfish (Lepomis MARGINATUS) and used a series of repeated-measures experiments to examine feeding performance (number of prey consumed, maximum prey size, and intra-oral transport time), digestive metabolism (specific dynamic action, SDA), and postprandial locomotor performance of snakes fed Ambystoma and Lepomis. Cost of digestion was similar between the prey types, likely reflecting their similar nutritional composition. However, snakes consumed larger Ambystoma than Lepomis and intra-oral transport time was much shorter for Ambystoma. Snakes fed Lepomis also suffered greater reduction in crawling speed than those fed Ambystoma. These differences highlight the need for behaviorally integrated approaches to understanding prey quality and support field observations of the importance of amphibian prey for juvenile watersnakes.

Needles in haystacks: Estimating detection probability and occupancy of rare and cryptic snakes

The species most in need of conservation or management are often also the most difficult to monitor, because of their rarity, secretive habits, or both. To combat these challenges, presence/absence (site occupancy) models can be used to track species occupancy at landscape scales. However, quantitative knowledge of detection probability (which is almost always <1) is required to reliably estimate site occupancy. Here, we present a case study that combines detection probabilities and site occupancy modeling to monitor a notoriously secretive guild of animals, North American aquatic snakes. Specifically, we use program PRESENCE to estimate detection probability ( p) and probability of site occupancy ( ψ) for seven snake species in relationship to site covariates, to understand the proximate and ultimate factors that influence habitat suitability. We were able to estimate p (3–46%) and ψ (12–96%) for each species and calculate the amount of unsuccessful effort necessary to declare absence of each species with statistical confidence (5–63 visits; 150–1890 trap-nights). We documented considerable interspecific variation in p and ψ; one species ( Nerodia fasciata) was widespread and highly detectable, while another ( Agkistrodon piscivorus) had low detectability despite its wide distribution. Five other species were secretive, or restricted to specific habitat types, or both, illustrating that complex and sometimes counterintuitive relationships exist between capture rate and occupancy. Incorporating p and ψ is essential to the success of large-scale monitoring programs for elusive species.

Ecological and methodological factors affecting detectability and population estimation in elusive species

AbstractAlthough mark‐recapture methods are among the most powerful tools for monitoring wildlife populations, the secretive nature of some species requires a comprehensive understanding of the factors that affect capture probability to maximize accuracy and precision of population parameter estimates (e.g., population size and survivorship). Here, we used aquatic snakes as a case study in applying rigorous mark‐recapture methods to estimate population parameters for secretive species. Specifically, we used intensive field sampling and robust design mark‐recapture analyses in Program MARK to test specific hypotheses about ecological and methodological factors influencing detectability of two species of secretive aquatic snakes, the banded watersnake (Nerodia fasciata), and the black swamp snake (Seminatrix pygaea). We constructed a candidate set of a priori mark‐recapture models incorporating various combinations of time‐ and sex‐varying capture and recapture probabilities, behavioral responses to traps (i.e., trap‐happiness or trap‐shyness), and temporary emigration, and we ranked models for each species using Akaike's Information Criterion. For both banded watersnakes and black swamp snakes we found strong support for time‐varying capture and recapture probabilities and strong trap‐happy responses, factors that can bias population estimation if not accommodated in the models. We also found evidence of sex‐dependent temporary emigration in black swamp snakes. Our study is among the first comprehensive assessments of factors affecting detectability in snakes and provides a framework for studies aimed at monitoring populations of other secretive species. © 2010 The Wildlife Society.

Seasonal Variation in the Spatial Ecology of the Banded Watersnake (Nerodia fasciata fasciata)

We used radiotelemetry to study the movements and habitat use in a population of Nerodia fasciata fasciata in the upper coastal plain of South Carolina from 2002 to 2006. Snakes that were surgically implanted with radiotransmitters were tracked during late spring of each year and located most days until the onset of hibernation in mid-November. Data were divided into summer and fall for seasonal analysis. Most home-range estimates and associated measures were significantly smaller during fall. Banded watersnakes used shoreline and littoral zone habitats in excess of their availability and used open water and terrestrial habitats relatively infrequently. Shoreline habitats were used more often during the fall, whereas littoral zone habitats were used more in the summer. Movement frequency was high relative to what has been reported for other Nerodia species. Females used shoreline habitats more than males, whereas males used littoral zone habitats more frequently.

Seasonal variation in terrestrial resource subsidies influences trophic niche width and overlap in two aquatic snake species: a stable isotope approach

Quantifying diet is essential for understanding the functional role of species with regard to energy processing, transfer, and storage within ecosystems. Recently, variance structure in the stable isotope composition of consumer tissues has been touted as a robust tool for quantifying trophic niche width, a task that has previously proven difficult due to bias in direct dietary analyses and difficulties in integrating diet composition over time. We used carbon and nitrogen stable isotope analyses to examine trophic niche width of two sympatric aquatic snakes, banded watersnakes Nerodia fasciata and black swamp snakes Seminatrix pygaea inhabiting an isolated wetland where seasonal migrations of amphibian prey cause dramatic shifts in resource availability. Specifically, we characterized snake and prey isotope compositions through time, space, and ontogeny and examined isotope values in relation to prey availability and snake diets assessed by gut content analysis. We determined that prey cluster into functional groups based on similarity of isotopic composition and seasonal availability. Isotope variance structure indicated that the trophic niche width of the banded watersnake was broader (more generalist) than that of the black swamp snake. Banded watersnakes also exhibited seasonal variation in isotope composition, suggesting seasonal diet shifts that track amphibian prey availability. Conversely, black swamp snakes exhibited little seasonal variation but displayed strong ontogenetic shifts in carbon and nitrogen isotope composition that closely paralleled ontogenetic shifts in their primary prey, paedomorphic mole salamanders Ambystoma talpoideum. Although niche dimensions are often treated as static, our results demonstrate that seasonal shifts in niche dimensions can lead to changes in niche overlap between sympatric species. Such short-term fluctuations in niche overlap can influence competitive interactions and consequently the composition and dynamics of communities and ecosystems.

Prey of the Broad-Banded Watersnake (Nerodia fasciata) and the Diamondback Watersnake (Nerodia rhombifer)

Abstract Stomach contents of Nerodia fasciata and Nerodia rhombifer from Louisiana and Texas were examined by either palpation or dissection. Recovered prey included one new prey item (Siren intermedia) for N. fasciata and one (Arius felis) for N. rhombifer. Prey:predator ratios of mass and total size of meals are reported.

Best of both worlds: Prey capture behaviour in banded watersnake (Nerodia fasciata)

Best of both worlds: Prey capture behaviour in banded watersnake (Nerodia fasciata)

Empirical Tests of Biased Body Size Distributions in Aquatic Snake Captures

Abstract Ecologists often rely on a suite of demographic parameters—such as age structure, body size distributions, population density, and sex ratios—to understand life history patterns, population dynamics, and community structure of snakes. Unfortunately, in many cases little consideration is given to how sampling techniques may influence the outcome of demographic studies. Herein, we use a combination of field capture techniques, an extensive database of field-captured snakes, and laboratory and field experiments to evaluate how capture methods may influence demographic assessments of several North American semi-aquatic snake species, including Agkistrodon piscivorus, Farancia abacura, Nerodia fasciata, N. floridana, N. rhombifer, N. taxispilota, Regina rigida, Seminatrix pygaea, and Thamnophis sauritus. We found that commercially available aquatic funnel traps (i.e., minnow traps) generally yielded biased assessments of population demography, but that the nature and magnitude of these biases varied p...

Comparative immunolocalization of Na+/K+‐ATPase and Na+/K+/2Cl− cotransporter in the kidneys of freshwater and marine snakes

In contrast with the marine sea snakes, watersnakes in the genus Nerodia are not known to have functional salt glands. Despite this physiological difference, at least two species of watersnake are known to inhabit marine environments; the remaining members of this genus occupy freshwater habitats. The mechanism by which marine watersnakes regulate ion balance without functional salt glands is unknown. In this study, we compared the cellular anatomy of kidneys from two species of watersnake, Nerodia fasciata (freshwater) and N. clarkii (marine), and one species of sea snake, Laticauda semifasciata (marine). Specifically, we examined the localization of Na+/K+‐ATPase (NKA) and Na+/K+/2Cl− cotransporter (NKCC), two proteins that are known to regulate membrane potential and drive salt secretion in all vertebrate secretory cells examined to date. Using histology and immunohistochemistry, we localized NKA and NKCC to the basolateral membranes of the distal tubules in all three species of snake. These results are consistent with the localization of these proteins in other secretory tissues such as the gills of teleost fishes and the salt glands of marine elasmobranchs, birds, and reptiles, and suggest a potential role for ion regulation at the level of the kidney. This research was funded by the National Geographic Society (8058‐06 to HBL) and the National Science Foundation (IOB‐0519579 to DHE).

Effects of flood suppression on natricine snake diet and prey overlap

Organisms may become adapted to disturbances when these disturbances occur periodically and at intermediate intensity. To investigate the effects of flood suppression, this study compared diet and competition of semi-aquatic snakes during flood (2000–2001) and no flood (2003–2005) years. Three natricine species, Nerodia erythrogaster (Forster in Bossu, 1771), Nerodia fasciata (L., 1766), and Thamnophis proximus (Say in James, 1823), were palpated for prey items in an east Texas floodplain under both conditions. Prey items were classified as crayfish, salamanders, anurans, or fish. Simpson’s diversity index of prey, frequency of consumed prey type, and prey importance values were compared between flood and no flood years. Pianka’s index of niche overlap was used to compare changes in diet overlap between species in the years with floods and those without. In the absence of floods, the number of prey types consumed by N. erythrogaster and T. proximus decreased. The frequency of prey types consumed during flood years was significantly different from the period of flood suppression for all three species. The order of prey importance also changed in the absence of floods for all three snake species. Without floods, diet overlap decreased between N. erythrogaster and the other two species; however, overlap between N. fasciata and T. proximus doubled.

Are ontogenetic shifts in diet linked to shifts in feeding mechanics?Scaling of the feeding apparatus in the banded watersnakeNerodia fasciata

The effects of size on animal behaviour, ecology, and physiology are widespread. Theoretical models have been developed to predict how animal form, function, and performance should change with increasing size. Yet, numerous animals undergo dramatic shifts in ecology (e.g. habitat use, diet) that may directly influence the functioning and presumably the scaling of the musculoskeletal system. For example, previous studies have shown that banded watersnakes (Nerodia fasciata) switch from fish prey as juveniles to frog prey as adults, and that fish and frogs represent functionally distinct prey types to watersnakes. We therefore tested whether this ontogenetic shift in diet was coupled to changes in the scaling patterns of the cranial musculoskeletal system in an ontogenetic size series (70-600 mm snout-vent length) of banded watersnakes. We found that all cranial bones and gape size exhibited significant negative allometry, whereas the muscle physiological cross-sectional area (pCSAs) scaled either isometrically or with positive allometry against snout-vent length. By contrast, we found that gape size, most cranial bones, and muscle pCSAs exhibited highly significant positive allometry against head length. Furthermore, the mechanical advantage of the jaw-closing lever system remained constant over ontogeny. Overall, these cranial allometries should enable watersnakes to meet the functional requirements of switching from fusiform fish to bulky frog prey. However, recent studies have reported highly similar allometries in a wide diversity of vertebrate taxa, suggesting that positive allometry within the cranial musculoskeletal system may actually be a general characteristic of vertebrates.

Visual acuity of the midland banded water snake estimated from evoked telencephalic potentials

The visual acuity of seven midland banded water snakes was measured by recording evoked responses from telencephalon to temporally modulated square wave grating patterns. Using conventional electrophysiological techniques and signal averaging, high contrast square wave gratings of different spatial frequencies were presented. Acuity was estimated by extrapolating relative response amplitude/log(10) spatial frequency functions which yielded an average acuity of 4.25 cycles/degree. Refractive state was also estimated by recording evoked potentials to intermediate spatial frequencies with different lenses in front of the eye. Polynomial fits indicated that under the experimental conditions the snakes were around 6.4 diopters hyperopic suggesting a corrected acuity of 4.89 cycles/degree. Reduction of grating luminance resulted in a reduction in evoked potential acuity measurements. These results indicate that the spatial resolution of midland banded water snakes is the equal of cat; about 20/120 in human clinical terms.

Post-drought responses of semi-aquatic snakes inhabiting an isolated wetland: Insights on different strategies for persistence in a dynamic habitat

Most aquatic habitats are temporally dynamic, and selection has favored diverse strategies to persist in the face of fluctuating environmental conditions. Isolated wetlands in the southeastern United States harbor high diversities of aquatic and semi-aquatic organisms. However, drought may render these wetlands temporarily unsuitable for many species, sometimes for years at a time. We studied the movement patterns and demography of seven species of semi-aquatic snakes at Ellenton Bay, an isolated 10-ha freshwater wetland in the Upper Coastal Plain of South Carolina, following complete drying of the bay during a drought from 2000 to 2003. Behavioral and population responses varied markedly among species. Cottonmouths (Agkistrodon piscivorus) migrated to and from the wetland annually, fared well, and reproduced during the drought. Banded watersnakes (Nerodia fasciata) suffered a dramatic population decline and apparently did not reproduce, while eastern green watersnakes (N. floridand) were locally extirpated. Black swamp snakes (Seminatrix pygaea) aestivated within the wetland and were less affected by the drought than Nerodia. Interspecific differences in response to drought demonstrate that conservation measures may affect species differently and highlight the importance of terrestrial habitat around wetlands for semi-aquatic reptiles.

Do juvenile gape‐limited predators compensate for their small size when feeding?

AbstractWhen juvenile and adult animals occur syntopically, juveniles are at a distinct performance disadvantage due to their absolutely small size. Yet, optimal foraging theory predicts that juvenile predators should feed efficiently in order to compete with adults for food, and to minimize their exposure to predators. Previous authors have suggested that one way for juvenile animals to accomplish these ecological tasks is by increasing their overall feeding performance relative to adults (compensation hypothesis). Nonetheless, only a handful of studies have tested whether juvenile animals have increased feeding performance (e.g. decreased ingestion and/or handling times relative to body size) compared with adults. We tested this hypothesis by examining the ontogeny of head dimensions and feeding performance (ingestion time and number of mandibular protractions) on fish prey for broad‐banded water snakesNerodia fasciata. Individuals were fed fish scaled in a 1:1 ratio to their head width. All head dimensions scaled with significant negative allometry versus body size, and thus smaller snakes had relatively larger heads for their body size compared with larger snakes. By contrast, most head variables (except head volume) exhibited positive allometry versus head length, demonstrating that larger snakes had larger head dimensions relative to head size compared with smaller snakes. In the performance trials, smaller snakes had worse feeding performances when feeding on similarly sized fish prey (relative to their head width) compared with larger snakes. Therefore, these data show that smaller water snakes do not compensate for their size through increased feeding performance.

Element Levels in Snakes in South Carolina: Differences Between a Control Site and Exposed Site on the Savannah River Site

Levels of 18 elements, including lead, mercury, selenium, and uranium, were examined in three species of snakes from an exposed and reference site on the Department of Energy's Savannah River Site in South Carolina. We tested the hypotheses that there were no differences as a function of species, and there were no difference between the exposed and control site for blood and muscle (tail) samples for banded water snake (Nerodia fasciata), brown water snake (N. taxispilota) and cotton mouth (Akistrodon piscivorous). The banded water snakes collected were significantly smaller than the other two species. For blood, there were significant species differences only for barium, copper, selenium, uranium and zinc, while for muscle tissue there were significant interspecific differences in aluminum, arsenic, barium, cobalt, cesium, copper, iron, lead, mercury, manganese, strontium, vanadium and zinc, suggesting that muscle tissue in the tail is a better indicator of potential interspecific differences. It is also easier logistically to collect tail tissue than blood. Where one species had significantly higher levels than the other species in muscle tissue levels, cottonmouth had higher levels of five elements (aluminum, cobalt, lead, mercury, vanadium), brown water snake had two (lead, strontium), and banded water snake had only barium. There were few significant differences between the control and reference site for levels of blood, but several for muscle tissue. All three species had significantly higher levels of arsenic and manganese at Tim's Branch than the reference site, and nickel and uranium were significantly higher for banded water snake and cotton mouth, the larger species. Individuals with high exposure of one element were exposed to high levels of other elements.

The functional meaning of “prey size” in water snakes (Nerodia fasciata, Colubridae)

The evolutionary success of macrostomatan (enlarged-gape) snakes has been attributed to their ability to consume large prey, in turn made possible by their highly kinetic skulls. However, prey can be "large" in several ways, and we have little insight into which aspects of prey size and shape affect skull function during feeding. We used X-ray videos of broad-banded water snakes (Nerodia fasciata) feeding on both frogs and fish to quantify movements of the jaw elements during prey transport, and of the anterior vertebral column during post-cranial swallowing. In a sample of additional individuals feeding on both frogs and fish, we measured the time and the number of jaw protractions needed to transport prey through the buccal cavity. Prey type (fish vs. frog) did not influence transport kinematics, but did influence transport performance. Furthermore, wider and taller prey induced greater movements of most cranial elements, but wider prey were transported with significantly less anterior vertebral bending. In the performance trials, heavier, shorter, and wider prey took significantly more time and a greater number of jaw protractions to ingest. Thus, the functional challenges involved in prey transport depend not only upon prey mass, but also prey type (fish vs. frog) and prey shape (relative height, width and length), suggesting that from the perspective of a gape-limited predator, the difficulty of prey ingestion depends upon multiple aspects of prey size.

Unveiling Escape and Capture Rates of Aquatic Snakes and Salamanders (Siren spp. and Amphiuma means) in Commercial Funnel Traps

ABSTRACT Aquatic funnel trapping with commercially available minnow traps has proven effective for sampling several aquatic snake species. However, the efficacy of this technique for sampling snakes has received little controlled evaluation. We investigated the ability of aquatic snakes to escape from three funnel trap varieties (cylindrical steel, cylindrical plastic, and rectangular collapsible nylon mesh). We found that when intentionally released into traps, the majority (74%) of snakes escaped within 24 hours. Snakes escaped most frequently from collapsible traps, and of the species tested, Seminatrix pygaea escaped most frequently. We found significant differences in capture rates among trap types for S. pygaea, Farancia abacura (both captured most in plastic traps), and Nerodia fasciata (captured most in steel traps). Additionally, as we captured many large aquatic salamanders (Siren spp. and Amphiuma means), we also report trapping efficacies of the funnel traps for these amphibians.