The British Herpetological Society

The Herpetological Journal is the Society's prestigious quarterly scientific journal. Articles are listed in Biological Abstracts, Current Awareness in Biological Sciences,Current Contents, Science Citation Index, and Zoological Record.

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Folder Volume 29, Number 3, July 2019

Volume 29, Number 3, July 2019

pdf 01. Genetic reconstruction of the invasion history of Anolis wattsi in Trinidad with a comment on the importance of ecological similarity to invasion success

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https://doi.org/10.33256/hj29.3.131137

pp. 131-137

Authors: Sozos N. Michaelides, Noah Gilbert, Brian E. Smith, Graham L. White, Adrian Hailey & Jason J. Kolbe

Abstract: Human activities have reshaped patterns of island biogeography for many groups of amphibians and reptiles. In Trinidad, an island in the West Indies with only one native Anolis lizard species, four additional anole species have been introduced since the 1800s. The most recent introduction, Anolis wattsi, native to Antigua, has become established despite the presence of multiple species of resident anoles. We used genetic data (mitochondrial DNA) to infer the geographic origin and genetic structure of introduced A. wattsi on Trinidad. We then gathered published data to compare eco-morphological traits of all anole species currently established on the island. We found three mtDNA haplotypes in Trinidad that clustered with two different clades from the northern part of the native range in Antigua, rejecting the hypothesis that the lizards originated in the pineapple-growing region of the south. However, a lack of fine-scale population structure precluded precise identification of the origin in Antigua of haplotypes introduced to Trinidad. Compared to the other anole species on Trinidad, A. wattsi is smaller, perches lower, and has a higher field body temperature. Thus, the successful establishment and spread of A. wattsi should not be surprising given the success of two previous introductions of anole species that were more similar ecomorphologically to the native species and each other, and the fact that Trinidad has relatively few anole species for its size.

Keywords: Anolis lizards; Caribbean islands; eco-morphological traits; invasions; mtDNA

pdf 02. The effect of thermal gradient design on the evaluation of thermoregulation in snakes

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https://doi.org/10.33256/hj29.3.138145

pp. 138-145

Authors: Ricardo Figueroa-Huitrón, Hibraim Adán Pérez-Mendoza, Aníbal Helios Díaz de la Vega-Pérez, Fausto Roberto Méndez-De la Cruz & Leticia Margarita Ochoa-Ochoa

Abstract: Hertz et al. (1993) designed what is now the most widely used protocol to analyse the thermal strategies and efficiency of small squamates. Preferred temperature range (Tp) is one of the most important variables required for determining the thermal efficiency index, and is calculated by monitoring the body temperature of the individuals in an enclosure containing a thermal gradient. Although thermoregulation studies of lizards have traditionally employed thermal gradients under laboratory conditions, this approach is not suitable for snakes given that such thermal gradients do not accurately represent their natural thermal environment and thus may result in snakes selecting suboptimal temperatures. Here, we compare the results of this thermal efficiency protocol using a laboratory thermal gradient (LG) and a semi-captivity thermal gradient (SCG) in the rattlesnake Crotalus polystictus. We found traces of seasonal variation in the SCG Tp, but this could not be assessed in the LG. Tp from the LG was much higher (29 – 34.3 °C) than from the SCG (22.5-30.9 °C). Values for the accuracy of thermoregulation (db) and thermal quality of the environment (de) indices from the LG were consistently higher than from the SCG. However, the efficiency of thermoregulation (E) was higher when calculated from the SCG. Tp estimates were wider than most that have been obtained from other snake species, suggesting that C. polystictus is eurythermic. The Blowin Demers and Weatherhead index was nearly identical in both gradients. Results from the LG indicated that C. polystictus is an inaccurate and inefficient thermoregulator, due to the higher temperatures chosen in this environment. In contrast, results from the SCG suggested that it is a highly accurate and active thermoregulator. We suggest that the LG could represent a stressful environment for snakes, and, as a consequence, they might select higher temperatures to increase anti-predatory performance at the expense of less efficient thermoregulation. Generally, a thermal gradient that more accurately replicates the natural habitat of snake species should reduce stress and result in more robust estimates of thermoregulatory variables.

Keywords: behaviour, Crotalus polystictus, preferred temperatures, snakes, refuges, thermal efficiency

pdf 03. Effects of environmental factors and conservation measures on a sand-dune population of the natterjack toad (Epidalea calamita) in north-west England: a 31-year study

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https://doi.org/10.33256/hj29.3.146154

pp. 146-154

Authors: Philip H. Smith & Graeme Skelcher

Abstract: A 31-year study monitored Britain’s largest natterjack toad population on the Sefton Coast sand-dune system in north-west England. Key objectives were to describe changes in numbers and breeding success, relate these to environmental variables and explore whether conservation efforts have been well targeted. Considerable variation was found in the number of water bodies used for spawning, the number of spawn strings laid and breeding success based on estimated toadlet production. There was a declining trend in annual totals of spawn strings and toadlets. Positive correlations were established between spring and April rainfall and both spawn count and toadlet production. April rainfall for the study area declined between 2000 and 2017. Premature desiccation of water bodies and associated poor breeding success were frequently observed, there being a positive relationship between water-table height and toadlet numbers. A long-term declining trend in the height of the water-table was established. The mean adult population of Sefton natterjacks was estimated at about 1200 individuals, with a peak around 3150. Successful breeding is increasingly reliant on management to excavate appropriately designed and managed “scrapes” that hold water long enough for metamorphosis to occur. Overgrowth of vegetation and loss of dynamism in the dune system threaten both the natural production of new breeding slacks and the natterjack’s open terrestrial habitat. Encouragement of dune dynamics by removing trees and scrub, increasing areas subject to livestock
grazing and mechanical rejuvenation may offer the best hope of conserving this species in the future.

Keywords: Amphibian; climate-change; rainfall; sand-dunes; vegetation-overgrowth; water-table

pdf 04. Dealing with hot rocky environments: Critical thermal maxima and locomotor performance in Leptodactylus lithonaetes (Anura: Leptodactylidae)

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https://doi.org/10.33256/hj29.3.155161

pp. 155-161

Authors: Iván Beltrán, Valeria Ramírez-Castañeda, Camilo Rodríguez-López, Eloisa Lasso & Adolfo Amézquita

Abstract: Environmental temperature has fitness consequences on ectotherm development, ecology and behaviour. Amphibians are especially vulnerable because thermoregulation often trades with appropriate water balance. Although substantial research has evaluated the effect of temperature in amphibian locomotion and physiological limits, there is little information about amphibians living under extreme temperature conditions. Leptodactylus lithonaetes is a frog allegedly specialised to forage and breed on dark granitic outcrops and associated puddles, which reach environmental temperatures well above 40 ˚C. Adults can select thermally favourable microhabitats during the day while tadpoles are constrained to rock puddles and associated temperature fluctuations; we thus established microhabitat temperatures and tested whether the critical thermal maximum (CTmax) of L. lithonaetes is higher in tadpoles compared to adults. In addition, we evaluated the effect of water temperature on locomotor performance of tadpoles. Contrary to our expectations, puddle temperatures were comparable and even lower than those temperatures measured in the microhabitats used by adults in the daytime. Nonetheless, the CTmax was 42.3 ˚C for tadpoles and 39.7 ˚C for adults. Regarding locomotor performance, maximum speed and maximum distance travelled by tadpoles peaked around 34 ˚C, approximately 1 ˚C below the maximum puddle temperatures registered in the puddles. In conclusion, L. lithonaetes tadpoles have a higher CTmax compared to adults, suggesting a longer exposure to extreme temperatures that lead to maintain their physiological performance at high temperatures. We suggest that these conditions are adaptations to face the strong selection forces driven by this granitic habitat.

Keywords: CTmax; thermal tolerance; tadpoles; granitic rocks; hot environment

pdf 05. Phylogenetic relationships and origin of the rattlesnakes of the Gulf of California islands (Viperidae: Crotalinae: Crotalus)

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https://doi.org/10.33256/hj29.3.162172

pp. 162-172

Authors: Eduardo Ruiz-Sanchez, Gustavo Arnaud, Oscar Roberto Cruz-Andrés & Francisco Javier Garcia-De León

Abstract: The islands of the Gulf of California are divided into three categories – oceanic, continental, and landbridge – and were formed from the Middle Miocene to the Holocene. The species of the Crotalus genus are an important ecological element of the endemic fauna of these islands. This study is the first to include several island-endemic species in a phylogenetic framework. We seek to understand the phylogenetic relationships among these species, and in particular, whether these species are more related to the Baja California peninsula or continental Mexican species, and whether the divergence times for these relationships are consistent with the formation of the islands. We performed a phylogenetic analysis and estimated divergence times using Bayesian inference and two mitochondrial 12S and 16S genes. The analyses show a new relationship between Crotalus angelensis and C. pyrrhus. Crotalus lorenzoensis was nested with C. ruber individuals, making this species a paraphyletic species. A novel relationship was also detected in that C. estebanensis was sister to C. basiliscus. The divergence time for all island-endemic Crotalus species is consistent with the formation of these islands. In addition, the insular species are related to their congeners in the Baja California peninsula or mainland Mexico.

Keywords: Baja California Peninsula; Bayesian inference; island-endemic; mtDNA; rattlesnakes

pdf 06. Observations of threatened Asian box turtles (Cuora spp.) on trade in Vietnam

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https://doi.org/10.33256/hj29.3.173178

pp. 173-178

Authors: Thong Pham Van, Benjamin Leprince, Hong Luong Xuan, Quyen Nguyen Thu, Olivier Le Duc, Cedric Bordes, Manh Vuong Tien & Luca Luiselli

Abstract: Asian box turtles (genus Cuora; Geoemydidae) are among the most threatened Asian turtles. Here, we present (i) a field investigation from 2014-2018 on the Cuora individuals traded by high-level traders in six provinces of Vietnam and (ii) the estimated numbers of traded individuals determined through interviews with traders. In addition, we (iii) provide an analysis of the confiscated individuals that were carried out at the main wildlife rescue centre of the Socialist Republic of Vietnam. Overall, the number of traded individuals observed was relatively small (n = 481), with C. bourreti being by far the most frequently observed in trade. During the same period, the interviewed traders estimated that about 3,400 individuals were traded through the period 2014-2018, most of them being C. bourreti. During 2010-2018, a total of 281 individuals were carried to the wildlife rescue centre, with over 60 % of the total rescued individuals being C. galbinifrons. Overall, the numbers of traded Cuora individuals recorded in the present study were very small compared to the huge estimates from other Asian countries. However, this lower traded number does not imply that the status’ of the target species are not affected, as their population sizes are already catastrophically reduced in Vietnam.


Keywords: turtle trade, Vietnam, interviews, field surveys

pdf 07. Urinary corticosterone metabolite responses to capture and visual elastomer tagging in the Asian toad (Duttaphrynus melanostictus)

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https://doi.org/10.33256/hj29.3.179183

pp. 179-183

Authors: Edward J. Narayan & Narahari P. Gramapurohit

Abstract: Herpetological research involving amphibians is increasingly using mark and recapture methods, employing various techniques such as toe-clipping and visible implant alphanumeric tags. Visual Implant Elastomer (VIE) is a new method available for herpetological surveys, involving a coloured dye inserted into the epidermal skin surface of frogs. Previously, there has been only one study which demonstrated that the VIE method does not generate a significant physiological stress response (using a faecal glucocorticoid method) in a captive amphibian species. Physiological stress can also be quantified non-invasively using urinary corticosterone metabolite (UCM) enzyme-immunoassay in amphibians. In this study, we tested the physiological stress response of a common amphibian species, wild caught Asian toads (Duttaphrynus melanostictus), by comparing UCM responses to capture handling, sham control or VIE marking method. Adult males (n = 38) were captured and sampled for baseline UCM (t = 0 h) then marked either using the VIE or sham (saline control), or only handled during capture. Subsequently, urine samples were collected at t = 2, 12 and 24 h for toads within each group. UCM levels were quantified using an enzyme-immunoassay (EIA) to determine differences among treatment groups and over time following capture. Toads generated acute stress responses to all three groups, showing a change in UCMs between baseline samples, 12 h, and 24 h samples. The mean UCM levels were not significantly different between the VIE method and the control groups (capture handling or sham operated). These results indicate that VIE method of tagging is no more stressful than routine handling of amphibians, hence in this context, the method does not have any additional welfare implications. Future research should explore the limitations of VIE tagging for long-term mark recapture studies, however, our current findings support its application as a minimally-invasive method for marking amphibians.


Keywords: amphibians, mark-recapture, welfare, stress, Visual Implant Elastomer (VIE)

pdf 08. Arm-wave display in a Liolaemus lizard

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https://doi.org/10.33256/hj29.3.184188

pp. 184-188

Author: Natalin S. Vicente

Abstract: Lizards show a great variety of visual displays. Among them, arm-waving is a behaviour that has received little attention and its role is still controversial. Here, I analyse the armwaves of Liolaemus pacha lizards in their natural habitat with the aim of determining their function. Arm-waving was performed by both sexes, usually with the ventral body surface in contact with the ground. Furthermore, it was more frequent when alone, and during female-male interactions. The results of this study are suggestive but not conclusive regarding the possible function of this behaviour.


Keywords: communication; predator-prey interaction; reptiles; social signal; submissive; visual display

pdf Supplementary Materials to article 1. Genetic reconstruction of the invasion history of Anolis wattsi in Trinidad with a comment on the importance of ecological similarity to invasion success

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Authors: Sozos N. Michaelides, Noah Gilbert, Brian E. Smith, Graham L. White, Adrian Hailey & Jason J. Kolbe

pdf Volume 29, Number 3, Full issue

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