Professor Richard Griffiths

Article

• Cayuela, H., Griffiths, R., Zakaria, N., Arntzen, J., Priol, P., Lena, J., Besnard, A. and Joly, P. (2020). Drivers of amphibian population dynamics and asynchrony at local and regional scales. Journal of Animal Ecology [Online]. Available at: https://doi.org/10.1111/1365-2656.13208.
  Abstract View in KAR
  Identifying the drivers of population fluctuations in spatially distinct populations remains a significant challenge for ecologists. Whereas regional climatic factors may generate population synchrony (i.e., the Moran effect), local factors including the level of density-dependence may reduce the level of synchrony. Although divergences in the scaling of population synchrony and spatial environmental variation have been observed, the regulatory factors that underlie such mismatches are poorly understood. Few previous studies have investigated how density-dependent processes and population-specific responses to weather variation influence spatial synchrony at both local and regional scales. We addressed this issue in a pond-breeding amphibian, the great crested newt (Triturus cristatus). We used capture-recapture data collected through long-term surveys in five T. cristatus populations in Western Europe. In all populations – and subpopulations within metapopulations – population size, annual survival and recruitment fluctuated over time. Likewise, there was considerable variation in these demographic rates between populations and within metapopulations. These fluctuations and variations appear to be context-dependent and more related to site-specific characteristics than local or regional climatic drivers. We found a low level of demographic synchrony at both local and regional levels. Weather has weak and spatially variable effects on survival, recruitment and population growth rate. In contrast, density-dependence was a common phenomenon (at least for population growth) in almost all populations and subpopulations. Our findings support the idea that the Moran effect is low in species where the population dynamics more closely depends on local factors (e.g. population density and habitat characteristics) than on large-scale environmental fluctuation (e.g. regional climatic variation). Such responses may have far-reaching consequences for the long-term viability of spatially structured populations and their ability to response to large-scale climatic anomalies.
• Nash, D., Humphries, N. and Griffiths, R. (2020). Effectiveness of translocation in mitigating reptile-development conflict in the UK. Conservation Evidence [Online] 17:7-11. Available at: https://www.conservationevidence.com/individual-study/7228.
  Abstract View in KAR
  The translocation of reptiles from development sites is a frequent but controversial intervention to resolve reptile-development conflicts. A general lack of post-translocation monitoring means that the fate of translocated reptiles is largely unknown. Here we report on the outcome of six reptile translocations carried out to mitigate the impacts of development. Through detailed post-translocation monitoring, we sought to determine whether translocated reptiles established populations within the receptor sites. To determine the effect of translocation, we investigated six sites within the UK that had received populations of translocated slow-worm Anguis fragilis, viviparous lizard Zootoca vivipara, adder Vipera berus and / or grass snake Natrix helvetica. Identification photographs were taken of all reptiles during the translocation. Following release, between one and three years of post-translocation monitoring was undertaken; during the monitoring, identification photographs were again collected to establish whether captured individuals were part of the translocated populations. Very few translocated individuals were encountered during the post-translocation monitoring. The mean number of translocated reptiles was 98 (SE 19.61). Of these, an average of 1.5 (SE 0.72) individuals or 1.6% of the population were captured during the monitoring. No recaptures of translocated reptiles were made at three (50%) of the study sites. The low recapture rates of translocated reptiles could be due to mortality, imperfect detection (including inaccurate identification of individuals) or post-translocation dispersal. There is some limited evidence to support each of the possible options, but post-translocation dispersal is considered to be the most likely explanation. The study found no confirmatory evidence that mitigation-driven translocations are compensating for the losses of populations to development.
• Griffin, J., Matechou, E., Buxton, A., Bormpoudakis, D. and Griffiths, R. (2019). Modelling environmental DNA data; Bayesian variable selection accounting for false positive and false negative errors. Journal of the Royal Statistical Society: Series C (Applied Statistics) [Online]. Available at: http://dx.doi.org/10.1111/rssc.12390.
  Abstract View in KAR
  Environmental DNA (eDNA) is a survey tool with rapidly expanding applications for assessing presence of a species at surveyed sites. eDNA methodology is known to be prone to false negative and positive errors at the data collection and laboratory analysis stage. Existing models for eDNA data require augmentation with additional sources of information to overcome identifiability issues of the likelihood function and do not account for environmental covariates that predict the probability of species presence or the proba-bilities of error. We present a novel Bayesian model for analysing eDNA data by proposing informative prior distributions for logistic regression coefficients that allow us to overcome parameter identifiability, while performing efficient Bayesian model-selection. Our methodology does not require the use of trans-dimensional algorithms and provides a general framework for performing Bayesian variable selection under informative prior distributions in logistic regression models.
• Canessa, S., Spitzen‐van der Sluijs, A., Stark, T., Allen, B., Bishop, P., Bletz, M., Briggs, C., Daversa, D., Gray, M., Griffiths, R., Harris, R., Harrison, X., Hoverman, J., Jervis, P., Muths, E., Olson, D., Price, S., Richards‐Zawacki, C., Robert, J., Rosa, G., Scheele, B., Schmidt, B. and Garner, T. (2019). Conservation decisions under pressure: Lessons from an exercise in rapid response to wildlife disease. Conservation Science and Practice [Online]. Available at: https://doi.org/10.1111/csp2.141.
  Abstract View in KAR
  Novel outbreaks of emerging pathogens require rapid responses to enable successful mitigation. We simulated a 1‐day emergency meeting where experts were engaged to recommend mitigation strategies for a new outbreak of the amphibian fungal pathogen Batrachochytrium salamandrivorans. Despite the inevitable uncertainty, experts suggested and discussed several possible strategies. However, their recommendations were undermined by imperfect initial definitions of the objectives and scope of management. This problem is likely to arise in most real‐world emergency situations. The exercise thus highlighted the importance of clearly defining the context, objectives, and spatial–temporal scale of mitigation decisions. Managers are commonly under pressure to act immediately. However, an iterative process in which experts and managers cooperate to clarify objectives and uncertainties, while collecting more information and devising mitigation strategies, may be slightly more time consuming but ultimately lead to better outcomes.
• Edwards, W., Griffiths, R., Bungard, M., Rakotondrasoa, E., Razafimanahaka, J., Razafindraibe, P., Andriantsimanarilafy, R. and Randrianantoandro, J. (2019). Microhabitat preference of the critically endangered golden mantella frog in Madagascar. Herpetological Journal [Online] 29:207-213. Available at: https://doi.org/10.33256/hj29.4.207213.
  Abstract View in KAR
  The golden mantella (Mantella aurantiaca) is a critically endangered (CR) frog, endemic to the eastern rainforests of Madagascar. Although the species is very popular in the pet trade and widely bred in captivity, its specific habitat requirements in the wild are poorly understood. Ten forested sites in the Moramanga district of Madagascar were surveyed for microhabitat and environmental variables, and the presence or absence of golden mantellas in quadrats positioned along transects in the vicinity of breeding sites. Mixed models were used to determine which variables best explained microhabitat use by golden mantellas. Sites where golden mantellas were found tended to have surface temperatures of 2023 ˚C, UVI units at about 2.9, about 30 % canopy cover, and around 30 % herbaceous cover. Within sites, golden mantellas preferred microhabitats that had 70 % leaf litter coverage and relatively low numbers of tree roots. This information can be used to improve the identification and management of habitats in the wild, as well as to refine captive husbandry needs
• Turner, H., Griffiths, R., Outerbridge, M. and Garcia, G. (2019). Estimating population parameters for the Critically Endangered Bermuda skink using robust design capture–mark–recapture modelling. Oryx [Online]. Available at: https://doi.org/10.1017/S0030605318001485.
  Abstract View in KAR
  Reliably estimating population parameters for highly secretive or rare animals is challenging. We report on the status of the two largest remaining populations of the Critically Endangered Bermuda skink Plestiodon longirostris, using a robust design capture–mark–recapture analysis. Skinks were tagged with passive integrated transponders on two islands and captured on 15 sampling occasions per year over 3 years. The models provided precise estimates of abundance, capture and survival probabilities and temporary emigration. We estimated skink abundance to be 547 ± SE 63.5 on Southampton Island and 277 ± SE 28.4 on Castle Island. The populations do not appear to be stable and fluctuated at both sites over the 3-year period. Although the populations on these two islands appear viable, the Bermuda skink faces population fluctuations and remains threatened by increasing anthropogenic activities, invasive species and habitat loss. We recommend these two populations for continued monitoring and conservation efforts.
• Worthington, H., McCrea, R., King, R. and Griffiths, R. (2019). Estimating Abundance from Multiple Sampling Capture-Recapture Data via a Multi-State Multi-Period Stopover Model. Annals of Applied Statistics [Online] 13:2043-2064. Available at: http://dx.doi.org/10.1214/19-AOAS1264.
  Abstract View in KAR
  Capture-recapture studies often involve collecting data on numerous capture occasions over a relatively short period of time. For many study species, this process is repeated, for example annually, resulting in capture information spanning multiple sampling periods. To account for the different temporal scales, the robust design class of models have traditionally been applied providing a frame-work in which to analyse all of the available capture data in a single likelihood expression. However, these models typically require strong constraints, either the assumption of closure within a sampling period (the closed robust design) or conditioning on the number of individuals captured within a sampling period (the open robust design). For real datasets these assumptions may not be appropriate. We develop a general modelling structure that requires neither assumption by explicitly modelling the movement of individuals into the population both within and between the sampling periods, which in turn permits the estimation of abundance within a single consistent framework. The exibility of the novel model structure is further demonstrated by including the computationally challenging case of multi-state data where there is individual time-varying discrete covariate information. We derive an efficient likelihood expression for the new multi-state multi-period stopover model using the hidden Markov model framework. We demonstrate the significant improvement in parameter estimation using our new modelling approach in terms of both the multi-period and multi-state components through both a simulation study and a real dataset relating to the protected species of great crested newts, Triturus cristatus.
• zu Ermgassen, S., Baker, J., Griffiths, R., Strange, N., Struebig, M. and Bull, J. (2019). The ecological outcomes of biodiversity offsets under “no net loss” policies: A global review. Conservation Letters [Online]. Available at: https://doi.org/10.1111/conl.12664.
  Abstract View in KAR
  No net loss (NNL) biodiversity policies mandating the application of a mitigation hierarchy (avoid, minimize, remediate, offset) to the ecological impacts of built infrastructure are proliferating globally. However, little is known about their effectiveness at achieving NNL outcomes. We reviewed the English-language peer-reviewed literature (capturing 15,715 articles), and identified 32 reports that observed ecological outcomes from NNL policies, including >300,000 ha of biodiversity offsets. Approximately one-third of NNL policies and individual biodiversity offsets reported achieving NNL, primarily in wetlands, although most studies used widely criticized area-based outcome measures. The most commonly cited reason for success was applying high offset multipliers (large offset area relative to the impacted area). We identified large gaps between the global implementation of offsets and the evidence for their effectiveness: despite two-thirds of the world’s biodiversity offsets being applied in forested ecosystems, we found none of four studies demonstrated successful NNL outcomes for forested habitats or species.We also found no evidence for NNL achievement using avoided loss offsets (impacts offset by protecting existing habitat elsewhere). Additionally, we summarized regional variability in compliance rates with NNL policies. As global infrastructural expansion accelerates, we must urgently improve the evidence-base around efforts to mitigate development impacts on biodiversity.
• Hudson, M., Griffiths, R., Martin, L., Fenton, C., Adams, S., Blackman, A., Sulton, M., Perkins, M., Lopez, J., Garcia, G., Tapley, B., Young, R. and Cunningham, A. (2019). Reservoir frogs: seasonality of Batrachochytrium dendrobatidis infection in robber frogs in Dominica and Montserrat. PeerJ [Online] 7. Available at: https://dx.doi.org/10.7717/peerj.7021.
  Abstract View in KAR
  Emerging infectious diseases are an increasingly important threat to wildlife conservation, with amphibian chytridiomycosis, caused by Batrachochytrium dendrobatidis, the disease most commonly associated with species declines and extinctions. However, some amphibians can be infected with B. dendrobatidis in the absence of disease and can act as reservoirs of the pathogen. We surveyed robber frogs (Eleutherodactylus spp.), potential B. dendrobatidis reservoir species, at three sites on Montserrat, 2011–2013, and on Dominica in 2014, to identify seasonal patterns in B. dendrobatidis infection prevalence and load (B. dendrobatidis genomic equivalents). On Montserrat there was significant seasonality in B. dendrobatidis prevalence and B. dendrobatidis load, both of which were correlated with temperature but not rainfall. B. dendrobatidis prevalence reached 35% in the cooler, drier months but was repeatedly undetectable during the warmer, wetter months. Also, B. dendrobatidis prevalence significantly decreased from 53.2% when the pathogen emerged on Montserrat in 2009 to a maximum 34.8% by 2011, after which it remained stable. On Dominica, where B. dendrobatidis emerged seven years prior to Montserrat, the same seasonal pattern was recorded but at lower prevalence, possibly indicating long-term decline. Understanding the dynamics of disease threats such as chytridiomycosis is key to planning conservation measures. For example, reintroductions of chytridiomycosis-threatened species could be timed to coincide with periods of low B. dendrobatidis infection risk, increasing potential for reintroduction success.
• Zhou, M., McCrea, R., Matechou, E., Cole, D. and Griffiths, R. (2019). Removal models accounting for temporary emigration. Biometrics [Online] 75:24-35. Available at: https://doi.org/10.1111/biom.12961.
  Abstract View in KAR
  Removal of protected species from sites scheduled for development is often a legal requirement in order to minimize the loss of biodiversity. The assumption of closure in the classic removal model will be violated if individuals become temporarily undetectable, a phenomenon commonly exhibited by reptiles and amphibians. Temporary emigration can be modeled using a multievent framework with a partial hidden process, where the underlying state process describes the movement pattern of animals between the survey area and an area outside of the study. We present a multievent removal model within a robust design framework which allows for individuals becoming temporarily unavailable for detection. We demonstrate how to investigate parameter redundancy in the model. Results suggest the use of the robust design and certain forms of constraints overcome issues of parameter redundancy. We show which combinations of parameters are estimable when the robust design reduces to a single secondary capture occasion within each primary sampling period. Additionally, we explore the benefit of the robust design on the precision of parameters using simulation. We demonstrate that the use of the robust design is highly recommended when sampling removal data. We apply our model to removal data of common lizards, Zootoca vivipara, and for this application precision of parameter estimates is further improved using an integrated model.
• Rosa, G., Bosch, J., Martel, A., Pasmans, F., Rebelo, R., Griffiths, R. and Garner, T. (2019). Sex‐biased disease dynamics increase extinction risk by impairing population recovery. Animal Conservation [Online]. Available at: http://dx.doi.org/10.1111/acv.12502.
  Abstract View in KAR
  The periodicity of life‐cycle events (phenology) modulates host availability to pathogens in a repeatable pattern. The effects of sexual differences in host phenology have been little explored in wildlife epidemiological studies. A recent series of ranavirosis outbreaks led to serious declines of Boscas’ newt populations at Serra da Estrela (Portugal). The peculiar phenology of this species, in which a large number of females remain in the aquatic habitat after the breeding season, turns it into a suitable model to test how sex‐biased mortality can affect host population persistence in the context of infectious diseases. We investigated how the phenology of Bosca's newt (i.e. biased number of females) mediated the impact of Ranavirus. We then evaluated the risk of extinction of the population under different scenarios of sex‐biased mortality using a population viability analysis. Two newt populations (one subject to yearly outbreaks and a comparative site where outbreaks have not been recorded) were tracked for trends over time following emergence of ranaviral disease, allowing us to assess the differential impact of the disease on both sexes. In addition to a significant decline in abundance of adult newts, our data suggest that phenology can affect disease dynamics indirectly, leading to reduction in females and a reversal of the sex ratio of the breeding population. Our models suggest that female‐biased mortality does not exacerbate Ranavirus‐driven population declines in the short‐term, but is likely to have a deleterious impact during the recovery process once the lethal effect of disease is removed from the system.
• Labisko, J., Griffiths, R., Chong-Seng, L., Bunbury, N., Maddock, S., Bradfield, K., Taylor, M. and Groombridge, J. (2019). Endemic, endangered, and evolutionarily significant: Cryptic lineages in Seychelles’ frogs. Biological Journal of the Linnean Society [Online] 126:417-435. Available at: https://doi.org/10.1093/biolinnean/bly183.
  Abstract View in KAR
  Cryptic diversity that corresponds with island origin has been previously reported in the endemic, geographically restricted sooglossid frogs of the Seychelles archipelago. The evolutionary pattern has not been fully explored, and given current amphibian declines and the increased extinction risk faced by island species, we sought to identify evolutionarily significant units (ESUs) to address conservation concerns for these highly threatened anurans. We obtained genetic data for two mitochondrial (mtDNA) and four nuclear (nuDNA) genes from all known populations of sooglossid frog (the islands of Mahé, Praslin, and Silhouette) to perform phylogenetic analyses and construct nuDNA haplotype networks. Bayesian and maximum likelihood analyses of mtDNA support monophyly and molecular differentiation of populations in all species that occur on multiple islands. Haplotype networks using statistical parsimony revealed multiple high-frequency haplotypes shared between islands and taxa, in addition to numerous geographically distinct (island-specific) haplotypes for each species. We consider each island-specific population of sooglossid frog as an ESU and advise conservation managers to do likewise. Furthermore, our results identify each island lineage as a candidate species, evidence for which is supported by Bayesian Poisson Tree Processes analyses of mtDNA, and independent analyses of mtDNA and nuDNA using the multispecies coalescent. Our findings add to the growing understanding of the biogeography and hidden diversity within this globally important region.
• Harper, L., Buxton, A., Rees, H., Bruce, K., Brys, R., Halfmaerten, D., Read, D., Watson, H., Sayer, C., Jones, E., Priestley, V., Mächler, E., Múrria, C., Garcés-Pastor, S., Medupin, C., Burgess, K., Benson, G., Boonham, N., Griffiths, R., Lawson Handley, L. and Hänfling, B. (2019). Prospects and challenges of environmental DNA (eDNA) monitoring in freshwater ponds. Hydrobiologia [Online] 826:25-41. Available at: https://doi.org/10.1007/s10750-018-3750-5.
  Abstract View in KAR
  Environmental DNA (eDNA) analysis is a rapid, non-invasive, cost-efficient biodiversity monitoring tool with enormous potential to inform aquatic conservation and management. Development is ongoing, with strong commercial interest, and new uses are continually being discovered. General applications of eDNA and guidelines for best practice in freshwater systems have been established, but habitat-specific assessments are lacking. Ponds are highly diverse, yet understudied systems that could benefit from eDNA monitoring. However, eDNA applications in ponds and methodological constraints specific to these environments remain unaddressed. Following a stakeholder workshop in 2017, researchers combined knowledge and expertise to review these applications and challenges that must be addressed for the future and consistency of eDNA monitoring in ponds. The greatest challenges for pond eDNA surveys are representative sampling, eDNA capture, and potential PCR inhibition. We provide recommendations for sampling, eDNA capture, inhibition testing, and laboratory practice, which should aid new and ongoing eDNA projects in ponds. If implemented, these recommendations will contribute towards an eventual broad standardisation of eDNA research and practice, with room to tailor workflows for optimal analysis and different applications. Such standardisation will provide more robust, comparable, and ecologically meaningful data to enable effective conservation and management of pond biodiversity.
• Dos Santos, M., Griffiths, R., Jowett, T., Rock, J. and Bishop, P. (2019). A comparison of understanding of the amphibian crisis by zoo visitors across three countries. Zoo Biology [Online]. Available at: https://doi.org/10.1002/zoo.21516.
  Abstract View in KAR
  Despite the global declines in the rate of amphibians, evaluation of public understanding of the crisis has not yet been carried out. We surveyed visitors (n = 1,293) at 15 zoos in Brazil, New Zealand, and the United Kingdom, using a certainty‐based assessment method to compare visitor knowledge of the global amphibian crisis. We further analyzed zoo educational material about amphibians to explore its potential to raise awareness through amphibian‐focused environmental education. Visitors in the three countries had relatively little understanding of amphibians and the global amphibian crisis. When the degree of confidence in answering the questions (high, medium, and low) is accounted for, correct answers varied between 28% and 39%. This compared to scores of between 58% and 73% when the degree of confidence in responding was not accounted for. However, specific areas of knowledge (e.g., biology, conservation, biogeography, and conceptual ideas) varied significantly across the countries. Visitors had a weaker grasp of biogeographical and conservation issues than general amphibian biology. Zoo visitors in Brazil knew less about amphibian conservation than those in New Zealand or the United Kingdom. There was less amphibian‐focused content in educational materials in zoos in Brazil than there was in the United Kingdom. Improving information about the global amphibian crisis may increase support for future conservation actions. Outreach education is one of the most important approaches in any strategic planning for conservation of species. Amphibian‐focused environmental education at institutions such as zoos and aquaria can be a crucial intervention to support amphibian conservation worldwide.
• Worthington, H., McCrea, R., King, R. and Griffiths, R. (2018). Estimation of population size when capture probability depends on individual state. Journal of Agricultural, Biological, and Environmental Statistics [Online] 24:154-172. Available at: https://dx.doi.org/10.1007/s13253-018-00347-x.
  Abstract View in KAR
  We develop a multi-state model to estimate the size of a closed population from capture–recapture studies. We consider the case where capture–recapture data are not of a simple binary form, but where the state of an individual is also recorded upon every capture as a discrete variable. The proposed multi-state model can be regarded as a generalisation of the commonly applied set of closed population models to a multi-state form. The model allows for heterogeneity within the capture probabilities associated with each state while also permitting individuals to move between the different discrete states. A closed-form expression for the likelihood is presented in terms of a set of sufficient statistics. The link between existing models for capture heterogeneity is established, and simulation is used to show that the estimate of population size can be biased when movement between states is not accounted for. The proposed unconditional approach is also compared to a conditional approach to assess estimation bias. The model derived in this paper is motivated by a real ecological data set on great crested newts, Triturus cristatus. Supplementary materials accompanying this paper appear online.
• Nash, D. and Griffiths, R. (2018). Ranging behaviour of adders (Vipera berus) translocated from a development site. Herpetological Journal [Online] 28:155-159. Available at: https://thebhs.org/publications/the-herpetological-journal/volume-28-number-4-october-2018/1852-04-ranging-behaviour-of-adders-i-vipera-berus-i-translocated-from-a-development-site.
  Abstract View in KAR
  Translocation of animals from sites scheduled for development is a widespread but controversial intervention to resolve human-wildlife conflicts. Indeed, reptiles are very frequently the subject of such translocations, but there is a paucity of information on the fate of such animals or how their behaviour compares to residents. In 2014, a population of adders (Vipera berus) was translocated from a development site in Essex, UK. A sample of snakes was fitted with external radio tags and tracked for a period of 10 days during the spring. This exercise was repeated during the summer using a combination of translocated and resident individuals. Translocated males exhibited significantly greater average daily movements than resident conspecifics. Furthermore, all translocated males undertook long-distance, unidirectional movements away from the release site. In contrast, all translocated females remained within 50 m of the point of release. One of the males returned to the donor site, crossing large areas of unsuitable habitat in doing so. Translocated males also maintained significantly larger total ranges than resident conspecifics. No differences in range sizes were observed between translocated and resident females. The dispersal of male snakes from the release site may increase the risk of mortality of translocated snakes and reduces the likelihood of establishing a new population. Interventions to encourage the establishment of new home ranges within the boundaries of release sites may include mechanisms to prevent dispersal immediately following release.
• Robinson, J., Fraser, I., St John, F., Randrianantoandro, J., Andriantsimanarilafy, R., Razafimanahaka, J., Griffiths, R. and Roberts, D. (2018). Wildlife supply chains in Madagascar from local collection to global export. Biological Conservation [Online] 226:144-152. Available at: https://dx.doi.org/10.1016/j.biocon.2018.07.027.
  Abstract View in KAR
  International trade in wildlife is a complex multi-billion dollar industry. To supply it, many animals are extracted from the wild, sourced from biodiversity-rich, developing countries. Whilst the trade has far-reaching implications for wildlife protection, there is limited information regarding the socio-economic implications in supply countries. Consequently, a better understanding of the costs and benefits of wildlife supply chains, for both livelihoods and conservation, is required to enhance wildlife trade management and inform its regulation. Using Madagascar as a case study, we used value chain analysis to explore the operation of legal wildlife trade on a national scale; we estimate the number of actors involved, the scale, value and profit distribution along the chain, and explore management options. We find that the supply of wildlife provided economic benefits to a number of actors, from local collectors, to intermediaries, exporters and national authorities. CITES-listed reptiles and amphibians comprised a substantial proportion of the quantity and value of live animal exports with a total minimum export value of 230,795USD per year. Sales prices of reptiles and amphibians increased over 100-fold between local collectors and exporters, with exporters capturing ~92% of final export price (or 57% when their costs are deducted). However, exporters shouldered the largest costs and financial risks. Local collectors obtained ~1.4% of the final sales price, and opportunities for poverty alleviation and incentives for sustainable management from the trade appear to be limited. Promoting collective management of species harvests at the local level may enhance conservation and livelihood benefits. However, this approach requires consideration of property rights and land-tenure systems. The complex and informal nature of some wildlife supply chains make the design and implementation of policy instruments aimed at enhancing conservation and livelihoods challenging. Nevertheless, value chain analysis provides a mechanism by which management actions can be more precisely targeted.
• Buxton, A., Groombridge, J. and Griffiths, R. (2018). Comparison of two Citizen Scientist Methods for Collecting Pond Water Samples for Environmental DNA Studies. Ctizen Science: Theory and Practice [Online] 3:2. Available at: https://doi.org/10.5334/cstp.151.
  Abstract View in KAR
  The use of environmental DNA (eDNA) for the survey of aquatic species offers a wide range of benefits over conventional surveys and has begun to be used by citizen scientists. One advantage of eDNA over conventional survey protocols is the comparative ease with which samples can be collected over a wide geographic area by citizen scientists. However, eDNA collection protocols vary widely between different studies, promoting a need to identify an optimum method. Collection protocols include ethanol precipitation and various filtration methods including those that use electronic vacuum or peristaltic pumps, hand pumps or syringes to capture eDNA on a membrane. We compare the effectiveness of two eDNA collection methods suitable for use by citizen scientists: glass-microfiber syringe filtration and ethanol precipitation. Paired samples of water were analysed for great crested newt (Triturus cristatus) DNA using (1) a laboratory tank experiment using different dilutions of water inoculated with newt DNA; and (2) by sampling naturally colonised ponds. Although syringe filters consistently yielded greater DNA extract concentrations in the tank experiments, this was not the case in samples collected from the field where no difference between the two methods was identified. Clearly, properties within the water – such as algae and particulate matter - can influence the amount of DNA captured by the two methods, so the sampling protocol of choice will depend on the design and goals of the study.
• Barata, I., Silva, E. and Griffiths, R. (2018). Predictors of abundance of a rare bromeliad-dwelling frog (Crossodactylodes itambe) in the Espinhaço Mountain Range of Brazil. Journal of Herpetology [Online] 52:321-326. Available at: http://dx.doi.org/10.1670/17-183.
  Abstract View in KAR
  Although tank bromeliads are used by many anuran species, bromeligenous frogs (species strictly dependent on bromeliads for reproduction) occur less frequently and are poorly understood. Crossodactylodes are small frogs confined to bromeliads where they lay their eggs and complete their life cycle without leaving the plant. The genus comprises five species and there is little information on their natural history. We focused on Crossodactylodes itambe – a species confined to a single summit of <0.5 km2 at 1700 m above sea level in the Espinhaço Mountain Range of Brazil. We surveyed frogs in 75 individual bromeliads during two consecutive years and we used a Generalized Linear Model to investigate the drivers of species abundance related to habitat structure and local climate. We recorded 446 adults, 267 tadpoles and 40 juveniles over the two years. Most bromeliads contained one adult frog and the mean number of tadpoles was 2-3. The structure of bromeliads influenced species abundance more than local climate. We found that bromeliad size, volume of central tank, and presence/absence of invertebrates and water influenced abundance of frogs. Abundance increased in larger bromeliads at higher elevation. Changes in the structure and size of bromeliads might therefore affect abundance. We provide the first species assessment and evaluation of threat categories for this poorly known species.
• Robinson, J., Griffiths, R., Fraser, I., Raharimalala, J., Roberts, D. and St. John, F. (2018). Supplying the wildlife trade as a livelihood strategy in a biodiversity hotspot. Ecology and Society [Online] 23:13. Available at: https//dx.doi.org/10.5751/ES-09821-230113.
  Abstract View in KAR
  Much of the global wildlife trade is sourced from biodiversity-rich developing countries. These often have high levels of poverty and habitat loss, particularly in rural areas where many depend on natural resources. However, wildlife collection may incentivize local people to conserve habitats that support their livelihoods. Here we examined the contribution of the commercial collection of live animals to rural livelihoods in Madagascar, one of the world’s most important biodiversity hotspots. Using questionnaires, we investigated the prevalence, profitability relative to other livelihood activities, and local importance of the trade, and its capacity to provide incentives for conservation. Thirteen percent of households were engaged in live animal collection in the study area (~5% trapped reptiles and amphibians and the remainder trapped invertebrates). This formed part of a diverse livelihood strategy, and was more profitable than other activities (in terms of returns per unit of effort), with median earnings of ~US$100 per season (~25% of Gross National Income per year). However, trapping was part-time, usually undertaken by poorer members of the community, and often perceived as opportunistic, risky, and financially unreliable. Further, trappers and nontrappers held similar perceptions regarding conservation, suggesting wildlife trade currently does not incentivize enhanced stewardship of traded species and their habitats. Our study brings together a range of methodologies to present the most comprehensive insights into livelihoods and conservation in poor rural communities involved in the commercial collection of live animals to supply international trade. This improved understanding of the wider socioeconomic dimensions of wildlife trade can inform policy and management interventions for both the threats and opportunities associated with global trade in biodiversity both in Madagascar and more generally.
• Austen, G., Bindemann, M., Griffiths, R. and Roberts, D. (2018). Species identification by conservation practitioners using online images: accuracy and agreement between experts. PeerJ [Online]. Available at: https://doi.org/10.7717/peerj.4157.
  Abstract View in KAR
  Emerging technologies have led to an increase in species observations being recorded via digital images. Such visual records are easily shared, and are often uploaded to online communities when help is required to identify or validate species. Although this is common practice, little is known about the accuracy of species identification from such images. Using online images of newts that are native and non-native to the UK, this study asked holders of great crested newt (Triturus cristatus) licences (issued by UK authorities to permit surveying for this species) to sort these images into groups, and to assign species names to those groups. All of these experts identified the native species, but agreement among these participants was low, with some being cautious in committing to definitive identifications. Individuals’ accuracy was also independent of both their experience and self-assessed ability. Furthermore, mean accuracy was not uniform across species (69–96%). These findings demonstrate the difficulty of accurate identification of newts from a single image, and that expert judgements are variable, even within the same knowledgeable community. We suggest that identification decisions should be made on multiple images and verified by more than one expert, which could improve the reliability of species data.
• Buxton, A., Groombridge, J. and Griffiths, R. (2018). Seasonal variation in environmental DNA detection in sediment and water samples. PlosOne [Online] 13:e0191737. Available at: https://doi.org/10.1371/journal.pone.0191737.
  Abstract View in KAR
  The use of aquatic environmental DNA (eDNA) to detect the presence of species depends
  on the seasonal activity of the species in the sampled habitat. eDNA may persist in sediments
  for longer than it does in water, and analysing sediment could potentially extend the
  seasonal window for species assessment. Using the great crested newt as a model, we
  compare how detection probability changes across the seasons in eDNA samples collected
  from both pond water and pond sediments. Detection of both aquatic and sedimentary
  eDNA varied through the year, peaking in the summer (July), with its lowest point in the winter
  (January): in all seasons, detection probability of eDNA from water exceeded that from
  sediment. Detection probability of eDNA also varied between study areas, and according to
  great crested newt habitat suitability and sediment type. As aquatic and sedimentary eDNA
  show the same seasonal fluctuations, the patterns observed in both sample types likely
  reflect current or recent presence of the target species. However, given the low detection
  probabilities found in the autumn and winter we would not recommend using either aquatic
  or sedimentary eDNA for year-round sampling without further refinement and testing of the
  methods.
• Mahoney, P., Miszkiewicz, J., Chapple, S., Le Luyer, M., Schlecht, S., Stewart, T., Griffiths, R., Deter, C. and Guatelli-Steinberg, D. (2018). The Biorhythm of Human Skeletal Growth. Journal of Anatomy [Online] 232:26-38. Available at: http://dx.doi.org/10.1111/joa.12709.
  Abstract View in KAR
  Evidence of a periodic biorhythm is retained in tooth enamel in the form of Retzius lines. The periodicity of Retzius lines (RP) correlates with body mass and the scheduling of life history events when compared between some mammalian species. The correlation has led to the development of the inter-specific Havers-Halberg Oscillation (HHO) hypothesis, which holds great potential for studying aspects of a fossil species biology from teeth. Yet, our understanding of if, or how the HHO relates to human skeletal growth is limited. The goal here is to explore associations between the biorhythm and two hard tissues that form at different times during human ontogeny, within the context of the HHO. First, we investigate the relationship of RP to permanent molar enamel thickness and the underlying daily rate that ameloblasts secrete enamel during childhood. Following this, we develop preliminary research conducted on small samples of adult human bone by testing associations between RP, adult femoral length (as a proxy for attained adult stature), and cortical osteocyte lacunae density (as a proxy for the rate of osteocyte proliferation). Results reveal RP is positively correlated with enamel thickness, negatively correlated with femoral length, but weakly associated with the rate of enamel secretion and osteocyte proliferation. These new data imply that a slower biorhythm predicts thicker enamel for children but shorter stature for adults. Our results develop the intra-specific HHO hypothesis suggesting that there is a common underlying systemic biorhythm that has a role in the final products of human enamel and bone growth.
• Ward, R., Griffiths, R., Wilkinson, J. and Cornish, N. (2017). Optimising monitoring efforts for secretive snakes: a comparison of occupancy and N-mixture models for assessment of population status. Scientific Reports [MS Excel] 7. Available at: http://dx.doi.org/10.1038/s41598-017-18343-5.
  Abstract View in KAR
  A fifth of reptiles are Data Deficient; many due to unknown population status. Monitoring snake populations can be demanding due to crypsis and low population densities, with insufficient recaptures for abundance estimation via Capture-Mark-Recapture. Alternatively, binomial N-mixture models enable abundance estimation from count data without individual identification, but have rarely been successfully applied to snake populations. We evaluated the suitability of occupancy and N-mixture methods for monitoring an insular population of grass snakes (Natrix helvetica) and considered covariates influencing detection, occupancy and abundance within remaining habitat. Snakes were elusive, with detectability increasing with survey effort (mean: 0.33 ± 0.06 s.e.m.). The probability of a transect being occupied was moderate (mean per kilometre: 0.44 ± 0.19 s.e.m.) and increased with transect length. Abundance estimates indicate a small threatened population associated to our transects (mean: 39, 95% CI: 20–169). Power analysis indicated that the survey effort required to detect occupancy declines would be prohibitive. Occupancy models fitted well, whereas N-mixture models showed poor fit, provided little extra information over occupancy models and were at greater risk of closure violation. Therefore we suggest occupancy models are more appropriate for monitoring snakes and other elusive species, but that population trends may go undetected.
• Barata, I., Griffiths, R. and Ridout, M. (2017). The power of monitoring: optimizing survey designs to detect occupancy changes in a rare amphibian population. Scientific Reports [Online] 7:1-9. Available at: http://dx.doi.org/10.1038/s41598-017-16534-8.
  Abstract View in KAR
  Biodiversity conservation requires reliable species assessments and rigorously designed surveys. However, determining the survey effort required to reliably detect population change can be challenging for rare, cryptic and elusive species. We used a tropical bromeliad-dwelling frog as a model system to explore a cost-effective sampling design that optimizes the chances of detecting a population decline. Relatively few sampling visits were needed to estimate occupancy and detectability with good precision, and to detect a 30% change in occupancy with 80% power. Detectability was influenced by observer expertise, which therefore also had an effect on the sampling design – less experienced observers require more sampling visits to detect the species. Even when the sampling design provides precise parameter estimates, only moderate to large changes in occupancy will be detected with reliable power. Detecting a population change of 15% or less requires a large number of sites to be surveyed, which might be unachievable for range-restricted species occurring at relatively few sites. Unless there is high initial occupancy, rare and cryptic species will be particularly challenging when it comes to detecting small population changes. This may be a particular issue for long-term monitoring of amphibians which often display low detectability and wide natural fluctuations.
• Pasmans, F., Bogaerts, S., Braeckman, J., Cunningham, A., Hellebuyck, T., Griffiths, R., Sparreboom, M., Schmidt, B. and Martel, A. (2017). Future of keeping pet reptiles and amphibians:towards integrating animal welfare, human health and environmental sustainability. Veterinary Record [Online] 181. Available at: http://doi: 10.1136/vr.104296.
  Abstract View in KAR
  The keeping of exotic pets is currently under debate and governments of several countries are increasingly exploring the regulation, or even the banning, of exotic pet keeping. Major concerns are issues of public health and safety, animal welfare and biodiversity conservation. The keeping of reptiles and amphibians in captivity encompasses all the potential issues identified with keeping exotic pets, and many of those relating to traditional domestic pets. Within the context of risks posed by pets in general, the authors argue for the responsible and sustainable keeping
  of reptile and amphibian pets by private persons, based on scientific evidence and on the authors' own expertise (veterinary medicine, captive husbandry, conservation biology).
• Meredith, H., St. John, F., Collen, B., Black, S. and Griffiths, R. (2017). Practitioner and scientist perceptions of successful amphibian conservation. Conservation Biology [Online] 32:366-375. Available at: http://dx.doi.org/10.1111/cobi.13005.
  Abstract View in KAR
  Conservation requires successful outcomes. However, success is perceived in many different ways depending on the desired outcome, which can vary according to numerous factors. We analysed perceptions of success among 355 scientists and practitioners working on amphibian conservation from over 150 organisations in more than 50 countries. Respondents identified four types of success: species and habitat improvements (84% of respondents); effective programme management (36%); outreach initiatives such as education and public engagement (25%); and the application of science-based conservation (15%). The most significant factor influencing overall perceived success was reducing threats. Capacity building was rated least important. Perceptions were influenced by experience, professional affiliation, involvement in conservation practice, and country of residence. More experienced conservation practitioners associated success with improvements to species and habitats, and less so with education and engagement initiatives. Whilst science-based conservation was rated as important, this factor declined in importance as the number of programmes a respondent participated in increased, particularly amongst those from Less Economically Developed Countries. The ultimate measure of conservation success – population recovery – may be difficult to measure in many amphibians, difficult to relate to the conservation actions intended to drive it, and difficult to achieve within conventional funding timeframes. The relaunched Amphibian Conservation Action Plan provides a framework for capturing lower-level processes and outcomes, identifying gaps, and measuring progress.
• Buxton, A., Groombridge, J. and Griffiths, R. (2017). Is the detection of aquatic environmental DNA influenced by substrate type?. PLOS ONE [Online] 12:e0183371. Available at: http://dx.doi.org/10.1371/journal.pone.0183371.
  Abstract View in KAR
  The use of environmental DNA (eDNA) to assess the presence-absence of rare, cryptic or invasive species is hindered by a poor understanding of the factors that can remove DNA from the system. In aquatic systems, eDNA can be transported out either horizontally in water flows or vertically by incorporation into the sediment. Equally, eDNA may be broken down by various biotic and abiotic processes if the target organism leaves the system. We use occupancy modelling and a replicated mesocosm experiment to examine how detection probability of eDNA changes once the target species is no longer present. We hypothesise that detection probability falls faster with a sediment which has a large number of DNA binding sites such as topsoil or clay, over lower DNA binding capacity substrates such as sand. Water removed from ponds containing the target species (the great crested newt) initially showed high detection probabilities, but these fell to between 40% and 60% over the first 10 days and to between 10% and 22% by day 15: eDNA remained detectable at very low levels until day 22. Very little difference in detection was observed between the control group (no substrate) and the sand substrate. A small reduction in detection probability was observed between the control and clay substrates, but this was not significant. However, a highly significant reduction in detection probability was observed with a topsoil substrate. This result is likely to have stemmed from increased levels of PCR inhibition, suggesting that incorporation of DNA into the sediment is of only limited importance. Surveys of aquatic species using eDNA clearly need to take account of substrate type as well as other environmental factors when collecting samples, analysing data and interpreting the results
• Buxton, A., Groombridge, J., Zakaria, N. and Griffiths, R. (2017). Seasonal variation in environmental DNA in relation to population size and environmentalfactors. Scientific Reports [Online] 7:46294. Available at: https://www.nature.com/articles/srep46294.
  Abstract View in KAR
  Analysing DNA that organisms release into the environment (environmental DNA, or eDNA) has
  enormous potential for assessing rare and cryptic species. At present the method is only reliably used
  to assess the presence-absence of species in natural environments, as seasonal influences on eDNA in
  relation to presence, abundance, life stages and seasonal behaviours are poorly understood. A naturally
  colonised, replicated pond system was used to show how seasonal changes in eDNA were influenced
  by abundance of adults and larvae of great crested newts (Triturus cristatus). Peaks in eDNA were
  observed in early June when adult breeding was coming to an end, and between mid-July and mid-
  August corresponding to a peak in newt larval abundance. Changes in adult body condition associated
  with reproduction also influenced eDNA concentrations, as did temperature (but not rainfall or UV).
  eDNA concentration fell rapidly as larvae metamorphosed and left the ponds. eDNA concentration
  may therefore reflect relative abundance in different ponds, although environmental factors can affect
  the concentrations observed. Nevertheless, eDNA surveys may still represent an improvement over
  unadjusted counts which are widely used in population assessments but have unreliable relationships
  with population size.
• Buxton, A., Groombridge, J., Zakaria, N. and Griffiths, R. (2017). Seasonal variation in environmental DNA in relation to population size and environmental factors. Scientific Reports [Online] 7:46294. Available at: http://dx.doi.org/10.1038/srep46294.
  Abstract View in KAR
  Analysing DNA that organisms release into the environment (environmental DNA, or eDNA) has
  enormous potential for assessing rare and cryptic species. At present the method is only reliably used
  to assess the presence-absence of species in natural environments, as seasonal influences on eDNA in
  relation to presence, abundance, life stages and seasonal behaviours are poorly understood. A naturally
  colonised, replicated pond system was used to show how seasonal changes in eDNA were influenced
  by abundance of adults and larvae of great crested newts (Triturus cristatus). Peaks in eDNA were
  observed in early June when adult breeding was coming to an end, and between mid-July and mid-
  August corresponding to a peak in newt larval abundance. Changes in adult body condition associated
  with reproduction also influenced eDNA concentrations, as did temperature (but not rainfall or UV).
  eDNA concentration fell rapidly as larvae metamorphosed and left the ponds. eDNA concentration
  may therefore reflect relative abundance in different ponds, although environmental factors can affect
  the concentrations observed. Nevertheless, eDNA surveys may still represent an improvement over
  unadjusted counts which are widely used in population assessments but have unreliable relationships
  with population size.
• Griffiths, R. (2017). Which amphibians should qualify for the ark?. Animal Conservation [Online] 20:120-121. Available at: http://dx.doi.org/10.1111/acv.12348.
  View in KAR
• Rosa, G., Sabino-Pinto, J., Laurentino, T., Martel, A., Pasmans, F., Rebelo, R., Griffiths, R., Stohr, A., Marschang, R., Price, S., Garner, T. and Bosche, J. (2017). Impact of asynchronous emergence of two lethal pathogens on amphibian assemblages. Scientific Reports [Online] 7:43260. Available at: http://dx.doi.org/10.1038/srep43260.
  Abstract View in KAR
  Emerging diseases have been increasingly associated with population declines, with co-infections
  exhibiting many types of interactions. The chytrid fungus (Batrachochytrium dendrobatidis) and
  ranaviruses have extraordinarily broad host ranges, however co-infection dynamics have been largely
  overlooked. We investigated the pattern of co-occurrence of these two pathogens in an amphibian
  assemblage in Serra da Estrela (Portugal). The detection of chytridiomycosis in Portugal was linked
  to population declines of midwife-toads (Alytes obstetricans). The asynchronous and subsequent
  emergence of a second pathogen - ranavirus - caused episodes of lethal ranavirosis. Chytrid effects
  were limited to high altitudes and a single host, while ranavirus was highly pathogenic across multiple
  hosts, life-stages and altitudinal range. This new strain (Portuguese newt and toad ranavirus – member
  of the CMTV clade) caused annual mass die-offs, similar in host range and rapidity of declines to other
  locations in Iberia affected by CMTV-like ranaviruses. However, ranavirus was not always associated
  with disease, mortality and declines, contrasting with previous reports on Iberian CMTV-like ranavirosis.
  We found little evidence that pre-existing chytrid emergence was associated with ranavirus and the
  emergence of ranavirosis. Despite the lack of cumulative or amplified effects, ranavirus drove declines
  of host assemblages and changed host community composition and structure, posing a grave threat to
  all amphibian populations.
• Matechou, E., McCrea, R., Morgan, B., Nash, D. and Griffiths, R. (2016). Open models for removal data. Annals of Applied Statistics [Online]. Available at: http://dx.doi.org/10.1214/16-AOAS949.
  Abstract View in KAR
  Individuals of protected species, such as amphibians and reptiles, often need to be removed from sites before development commences. Usually, the population is considered to be closed. All individuals are assumed to i) be present and available for detection at the start of the study period and ii) remain at the site until the end of the study, unless they are detected. However, the assumption of population closure is not always valid. We present new removal models which allow for population renewal through birth and/or immigration, and population depletion through sampling as well as through death/emigration. When appropriate, productivity may be estimated and a Bayesian approach allows the estimation of the probability of total population depletion. We demonstrate the performance of the models using data on common lizards, Zootoca vivipara, and great crested newts, Triturus cristatus.
• Austen, G., Bindemann, M., Griffiths, R. and Roberts, D. (2016). Species identification by experts and non-experts: comparing images from field guides. Scientific Reports [Online] 6. Available at: http://dx.doi.org/10.1038/srep33634.
  Abstract View in KAR
  Accurate species identification is fundamental when recording ecological data. However, the ability to correctly identify organisms visually is rarely questioned. We investigated how experts and non-experts compared in the identification of bumblebees, a group of insects of considerable conservation concern. Experts and non-experts were asked whether two concurrent bumblebee images depicted the same or two different species. Overall accuracy was below 60% and comparable for experts and non-experts. However, experts were more consistent in their answers when the same images were repeated, and more cautious in committing to a definitive answer. Our findings demonstrate the difficulty of correctly identifying bumblebees using images from field guides. Such error rates need to be accounted for when interpreting species data, whether or not they have been collected by experts. We suggest that investigation of how experts and non-experts make observations should be incorporated into study design, and could be used to improve training in species identification.
• Hudson, M., Young, R., D’Urban Jackson, J., Orozco-terWengel, P., Martin, L., James, A., Sulton, M., Garcia, G., Griffiths, R., Thomas, R., Magin, C., Bruford, M. and Cunningham, A. (2016). Dynamics and genetics of a disease driven species decline to near extinction: lessons for conservation. Scientific reports [Online] 6. Available at: http://dx.doi.org/10.1038/srep30772.
  Abstract View in KAR
  Amphibian chytridiomycosis has caused precipitous declines in hundreds of species worldwide. By tracking mountain chicken (Leptodactylus fallax) populations before, during and after the emergence of chytridiomycosis, we quantified the real-time species level impacts of this disease. We report a range-wide species decline amongst the fastest ever recorded, with a loss of over 85% of the population in fewer than 18 months on Dominica and near extinction on Montserrat. Genetic diversity declined in the wild, but emergency measures to establish a captive assurance population captured a representative sample of genetic diversity from Montserrat. If the Convention on Biological Diversity’s targets are to be met, it is important to evaluate the reasons why they appear consistently unattainable. The emergence of chytridiomycosis in the mountain chicken was predictable, but the decline could not be prevented. There is an urgent need to build mitigation capacity where amphibians are at risk from chytridiomycosis.
• Wombwell, E., Garner, T., Cunningham, A., Quest, R., Pritchard, S., Rowcliffe, J. and Griffiths, R. (2016). Detection of Batrachochytrium dendrobatidis in amphibians imported into the UK for the pet trade. EcoHealth [Online]. Available at: http://dx.doi.org/10.1007/s10393-016-1138-4.
  Abstract View in KAR
  There is increasing evidence that the global spread of the fungal pathogen Batrachochytrium dendrobatidis (Bd) has been facilitated by the international trade in amphibians. Bd was first detected in the UK in 2004, and has since been detected in multiple wild amphibian populations. Most amphibians imported into the UK for the pet trade from outside the European Union enter the country via Heathrow Animal Reception Centre (HARC), where Bd positive animals have been previously detected. Data on the volume, diversity and origin of imported amphibians were collected for 59 consignments arriving at HARC between November 2009 and June 2012, along with a surveillance study to investigate the prevalence of Bd in these animals. Forty three amphibian genera were recorded, originating from 12 countries. It was estimated that 5000 – 7000 amphibians are imported through HARC into the UK annually for the pet trade. Bd was detected in consignments from the USA and Tanzania, in six genera, resulting in an overall prevalence of 3.6%. This suggests that imported amphibians are a source of Bd within the international pet trade.

Datasets / databases

• Austen, G., Bindemann, M., Griffiths, R. and Roberts, D. (2018). Species identification by conservation practitioners using online images: accuracy and agreement between experts. [MS Excel file]. Available at: http://dx.doi.org/10.7717/peerj.4157.
  Abstract View in KAR
  Emerging technologies have led to an increase in species observations being recorded via digital images. Such visual records are easily shared, and are often uploaded to online communities when help is required to identify or validate species. Although this is common practice, little is known about the accuracy of species identification from such images. Using online images of newts that are native and non-native to the UK, this study asked holders of great crested newt (Triturus cristatus) licences (issued by UK authorities to permit surveying for this species) to sort these images into groups, and to assign species names to those groups. All of these experts identified the native species, but agreement among these participants was low, with some being cautious in committing to definitive identifications. Individuals’ accuracy was also independent of both their experience and self-assessed ability. Furthermore, mean accuracy was not uniform across species (69–96%). These findings demonstrate the difficulty of accurate identification of newts from a single image, and that expert judgements are variable, even within the same knowledgeable community. We suggest that identification decisions should be made on multiple images and verified by more than one expert, which could improve the reliability of species data.
• Austen, G., Bindemann, M., Griffiths, R. and Roberts, D. (2016). Species identification by experts and non-experts: comparing images from field guides. [Electronic deposit (Excel)].
  Abstract View in KAR
  Accurate species identification is fundamental when recording ecological data. However, the ability to correctly identify organisms visually is rarely questioned. We investigated how experts and non-experts compared in the identification of bumblebees, a group of insects of considerable conservation concern. Experts and non-experts were asked whether two concurrent bumblebee images depicted the same or two different species. Overall accuracy was below 60% and comparable for experts and non-experts. However, experts were more consistent in their answers when the same images were repeated, and more cautious in committing to a definitive answer. Our findings demonstrate the difficulty of correctly identifying bumblebees using images from field guides. Such error rates need to be accounted for when interpreting species data, whether or not they have been collected by experts. We suggest that investigation of how experts and non-experts make observations should be incorporated into study design, and could be used to improve training in species identification.

Monograph

• Bormpoudakis, D., Foster, J., Gent, T., Griffiths, R., Russell, L., Starnes, T., Tzanopoulos, J. and Wlikinson, J. (2016). Developing Models to Estimate the Occurrence in the English Countryside of Great Crested Newts, a Protected Species under the Habitats Directive. Defra. Available at: http://randd.defra.gov.uk/Default.aspx?Menu=Menu&Module=More&Location=None&ProjectID=19272&FromSearch=Y&Publisher=1&SearchText=WC1108&SortString=ProjectCode&SortOrder=Asc&Paging=10.
  Abstract View in KAR
  The great crested newt is a European Protected Species (EPS) with a widespread distribution within Great Britain. This results in the species frequently coming into conflict with development. Consequently, decision-makers in local government and licensing authorities face complex issues when it comes to reconciling development and conservation. New approaches are therefore needed to ensure that conservation decisions are based upon the best available science. The project set out to evaluate new potential approaches to these issues using three work packages: (1) Develop, test and compare species distribution models (SDMs) for great crested newts; (2) Building on these models, develop a methodology for assessing the impact of a plan or project on the local conservation status of great crested newts; and (3) End-user testing to assess model applications and fitness for purpose. Defra commissioned the project with additional funding from Natural Resources Wales, and together with Natural England and JNCC, also provided guidance.
  GLM models developed using eDNA presence-absence data for a small area of Kent provided a good prediction of the county-wide distribution of the species. GLM models developed for Cheshire and Lincolnshire using eDNA data yielded weaker models. Equally, the Kent model did not reliably fit Cheshire and Lancashire, suggesting that the predictor variables vary geographically.
  Maxent and ensemble models yielded good fits to county-wide distributions but poor fits to the localised eDNA data in all three counties. These models may have utility at a broad scale, but cannot account for absences at a local scale. Equally, some important variables at a local scale cannot be obtained through GIS layers and need to be obtained through field surveys. Constructing models for different scales therefore requires different modelling tools and different types of predictor variables.
  Maxent models of the national distribution of great crested newts in England gave predictions that were broadly consistent with current knowledge and can be used to calculate potential areas of occupancy.
  A framework for assigning and measuring Favourable Reference Values (FRVs) for great crested newts at different scales was developed using both an ‘equilibrium’ (=’no net change’) approach and FRVs set using baseline data according to other criteria. These principles were combined with SDMs and connectivity analysis of five case studies. The case studies combine both real and hypothetical data, and illustrate how a modelling approach can be used to identify important areas of newt habitat, identify connectivity between ponds, predict potential impacts of development, and design and evaluate mitigation measures.
  Three end-user consultation exercises showed that there was considerable interest and enthusiasm for the development and application of SDMs across a range of applications and stakeholders. Concerns were expressed over the quality and quantity of data available for modelling using current data-flow systems; the predictive power of models; and the potential for model outputs to be misused. Challenges that need to be addressed include training, expertise and building capacity, enhancing the regulatory framework for protected species, and the improvement and centralisation of data management systems.
  Species Distribution Models (SDMs) provide an objective and evidence-based tool for use within decision-making processes involving great crested newts. They have the potential to identify priority areas for conservation, target survey effort, assess the impacts of development, and assign Favourable Reference Values for the species. However, great crested newt records and habitat data are currently dispersed across multiple recording systems and vary in quality and quantity. A well-integrated data management system is required if SDMs are to make the best use of available information.

Thesis

• Edwards, W. (2019). Conservation of the Golden Mantella in Madagascar: Integrating in Situ and Ex Situ Research.
  Abstract View in KAR
  The greatest threats to biodiversity in Madagascar are habitat destruction, fragmentation and climate change. Complementary in situ and ex situ research can aid conservation because many aspects of natural history that can usefully inform conservation measures are difficult to study in the field. The golden mantella is an excellent model as it is unique in that it is a charismatic, high profile Critically Endangered amphibian, but is abundant in captivity and highly suitable for ex situ research. In situ research in a new protected area of Madagascar found surface temperature, litter coverage and the number of tree roots were the most important predictor variables associated with quadrats occupied by golden mantellas. Microclimatic measurements made in the field informed the design of the replicated climatic-controlled enclosures (Froggotrons) for golden mantellas at Paignton Zoo.
  Froggotrons revealed golden mantellas had a bimodal activity pattern during daylight hours even under different temperature regimes. At lower temperatures (16 ºC - 19 ºC) mantellas were overall less active than those at higher temperatures (20 ºC - 25 ºC), but the phasing and bimodal nature of the activity rhythm was the same under both temperature regimes. Most activity occurred when humidity levels exceeded 85%. Golden mantellas were most active, spent most time in the open and less time on leaves at 21.5 ºC. Where temperature deviated either way from 21.5 ºC there was an associated decrease in activity and an increased tendency to hide in leaves. Results also show that even under optimum temperature and humidity regimes less than 50% of the frogs were active in open areas at any one time. Ex situ results have been used to assist with the design and timing of field population assessments and shed light on issues concerning imperfect detection when applying models to assess abundance. Species distribution modelling results suggest a potential south-eastwardly shift away from current distribution range and a decrease in suitable habitat from 2110 km2 under current climate to between 112 km2-138 km2 by the year 2085. Golden mantella research is a new development in the area of collaborative, complementary conservation. Integrating in situ and ex situ research may help mitigate the multi-faceted and synergistic threats to biodiversity in Madagascar.
• Buxton, A. (2018). Population Assessment of Great Crested Newts Using Environmental DNA.
  Abstract View in KAR
  Targeting environmental DNA (eDNA) for species monitoring and biodiversity assessment is a newly emerged technique. Surveys targeting eDNA involve the isolation of DNA shed into the environment by an organism to identify species utilizing a particular location. Despite uncertainties surrounding the technique, eDNA has begun to be used extensively for species assessments. Using the great crested newt (Triturus cristatus) as a model species, we (1) determined seasonal trends in eDNA with a view to optimising survey timing; (2) estimated the detection probabilities for eDNA and their covariates; and (3) explored how abundance estimates may be made from aquatic eDNA samples.
  
  We conclude that detection varies through the year, with most reliable detection coinciding with peak breeding. However, outside the breeding season detection is possible where larval numbers are high. Environmental and population factors may influence release of DNA from a target species or eDNA persistence in water and sediments. These include sediment type, number of both adults and larvae, changes in adult body condition, habitat variables and sampling location. As many external covariates were found to influence eDNA concentration, it would not be appropriate to use eDNA concentration as a predictor of abundance. However; we apply a modelling approach to generate estimates of abundance using genomic DNA, with a degree of accuracy deemed acceptable for ecological monitoring.
  
  The conclusions are directly relevant to refining survey design and analysis for the assessment of great crested newt populations. The results are also applicable more generally to the eDNA survey method, its development, survey design and interpretation, whether for single species analysis or community analysis.
• Ward, R. (2017). Status and Conservation of the Grass Snake in Jersey.
  Abstract View in KAR
  Global biodiversity losses are being driven by anthropogenic pressures; the most pervasive of which is habitat loss resulting in fragmentation and population isolation. These issues are prevalent throughout Europe due to high intensity agriculture and increasing human population densities. Limitations imposed by resources and the secretive lifestyles of many species hinder the ability of conservationists to undertake status assessments and identify conservation actions. This thesis investigates the threats to an isolated population of grass snakes Natrix helvetica on the island of Jersey, providing recommendations for conservation management and recovery, whilst testing the suitability of tools for monitoring cryptic species. Grass snakes were historically widespread throughout Jersey; however, anthropogenic influences have restricted their distribution to the west and southwest. Furthermore, recent monitoring efforts have detected few individuals and their status is unknown.
  Intensive surveys to locate individuals combined with occupancy and N-mixture (abundance) models identified continued occupancy of semi-natural sites in the island's west and southwest, but also highlighted poor detectability of the species unless utilising a large survey effort. Therefore, a large amount of effort is required to determine absence of snakes, and declines in the population cannot be detected with reasonable power. Occupancy models were more reliable than N-mixture models, particularly due to the risks of closure violation when estimating abundance. Nonetheless, N-mixture models estimated an abundance of 48 snakes (95% CI: 23?1279) across the study sites. Radio-tracking also provided evidence for low detection rates. Additionally snakes demonstrated small ranges (mean: 2.48 ha ± 3.54 SD), site fidelity, preferences for ranges close to paths and compost heaps, but avoided crossing roads. Snakes were positively associated with structurally complex habitats including rough grassland, dense scrub and gorse at multiple spatial scales, but negatively with open and wooded habitats.
  Species distribution modelling indicated similar habitat preferences to radio-tracking and poor suitability of agricultural habitats. Areas close to amphibian prey populations were also suitable whereas those with high road densities were not. A fifth of Jersey contained priority conservation areas, however almost 90% of these areas do not receive statutory protection. Those in the west and southwest should be prioritised for protection due to their proximity to extant subpopulations. Mitochondrial genes identified the population to belong to a western lineage of grass snakes Natrix helvetica helvetica, with a probable natural colonisation prior to separation from northwest France. Within Jersey, microsatellite markers identified three subpopulations, with significant differentiation between snakes in the south and west. This coincides with a dense urban area, through which connectivity needs improvement.
  The Jersey grass snake population can be classified as regionally Vulnerable (D2) under IUCN guidelines. The study illustrates how nature reserves are important for maintaining isolated subpopulations and the potential avenues by which statutory protection, sympathetic management practices and efforts to improve inter-reserve connectivity can contribute to conservation objectives.
• Thompson, D. (2017). Effects of Climate Change on the Breeding Phenology of Newts.
  Abstract View in KAR
  Phenological advancements have been documented in a variety of taxa in response to climate change. Amphibians have mostly been studied in the northern hemisphere with the majority of responses suggesting an advancement in breeding dates in line with increasingly warmer spring temperatures. This study looked at various aspects of the breeding phenology of palmate, smooth and great crested newts at two neighbouring metapopulations in Canterbury, Kent, UK over a period of 20 years. Median date (seasonality), duration of aquatic period and individual body condition were analysed to identify any changes over time and then again to identify any relationships with climatic factors. The responses varied between pond and species: great crested newts showed a delay in median capture date and a lengthening in duration of aquatic period at two out of five ponds, plus an increase in body condition; palmate newts showed a delay in median capture and lengthening of duration at one pond; and smooth newts showed a lengthening in duration at two of the five ponds. There does appear to be a relationship with climate, but as the changes in phenology were not observed at all ponds within the same local climatic region, it suggests that the effects of climate change may be indirect, and local conditions may compensate or override any potential climate-related effects. This study is the first to document delayed breeding activity in great crested and palmate newts, and the first for urodeles in Europe. These contrasting results show that amphibians are responding to environmental changes at a population level and therefore climate change mitigation measures may need to be population-specific.
• Nash, D. (2017). An Assessment of Mitigation Translocations for Reptiles at Development Sites.
  Abstract View in KAR
  All native reptile species are protected against harm through their inclusion on UK legislation. With the exception of two species, this protection does not extend to reptile habitat. As a result, reptiles are frequently subject to mitigation translocations to facilitate the development of land. However, there are few published studies of the effects of mitigation translocation on reptile populations and whether such translocations are effective conservation interventions. The effectiveness of translocation was tested through a combination of: 1) field surveys of sites subject to mitigation across England and Wales; 2) the radio tracking of translocated adders; 3) the monitoring of a population of slow-worms at site where they were released 20 years ago; and 4) a penning experiment to test whether viviparous lizards attempt to disperse from the release site.
  
  Very few translocated reptiles were encountered during the monitoring of release sites. This paucity of recaptures is either due to post-release mortality, imperfect detection or dispersal. Translocated male adders dispersed farther and had larger home range sizes than resident conspecifics. Some male adders undertook large unidirectional migrations back to the donor site crossing areas of unsuitable habitat as they did so. A population of slow-worms persisted at an isolated site two decades after translocation, albeit in relatively small numbers. Body condition improved over 20 years and the population resumed breeding and recruitment. The temporary penning of viviparous lizards was effective in preventing post-release dispersal and resulted in an increase in recapture rates of greater than 16 times when compared to unpenned viviparous lizard populations. The fact that no lizards were recaptured in the unpenned areas provides strong evidence for the effect of post-release dispersal. Although, mitigation translocations may prevent the immediate death of animals that would otherwise be destroyed with their habitat, there is little evidence that they are compensating for the loss of populations on a broad scale.
• Moss, A. (2017). The Educational Value of Zoos and Aquariums.
  Abstract View in KAR
  Zoos and aquariums are some of the most-visited institutions, with around 700 million visits made to them globally each year. They are, in a basic sense, simply repositories of living biodiversity. However, the justifications for the continued existence of zoos have evolved since their inception in the late 18th and early 19th centuries, and nearly all now position themselves as organisations focussed on the conservation of the world's remaining biodiversity. Public education of visitors is seen as, and is claimed to be, a central role in achieving this mission. Until relatively recently, very little was known about the impacts of zoo-based education. In this thesis, I will argue that good, progressive zoos and aquariums can and do achieve positive educational impacts on the people that visit them. Using a combination of structured observational methods and traditional social survey designs, I have explored the relative popularity of zoo animals, assessed the tolerance of zoo visitors to different environmental education themes, and have conducted the first fully global evaluation of zoo education impacts. In brief, I found that taxonomic group (mammals), increasing body size and activity levels were significant predictors of visitor interest in zoo animals, giving zoo professionals an evidence base to make decisions regarding education programming and exhibit design. Zoo visitors were also found to be, in the main, accepting to education content that reached beyond animal-based themes. This gives zoo educators the evidence to support their efforts to design and deliver more diverse programmes that cover wider environmental education themes. Finally, from a global survey of more than 5,000 visitors to 26 zoos and aquariums, I concluded that people tend to end their visit with a significantly greater understanding of what biodiversity is, as well as the ways that they personally can help protect it. The links between these two knowledge strands were, however, found to be less strong than predicted, leading to a discussion around the significance of the role of knowledge in catalysing human behaviour change. Aside from demonstrating their own positive educational impact, the wider implication of this research is that zoos and aquariums can also show that they are helping to achieve global biodiversity targets; namely, UN Aichi Biodiversity Target 1. From this, I will argue that the educational role of zoos should be considered as a more influential contributor to biodiversity conservation, and society more generally, than has previously been accepted.
• Robinson, J. (2017). Supplying the Exotic Pet Trade: Conservation and Livelihood Implications.
  Abstract View in KAR
  The wildlife trade represents a significant threat to biodiversity, but may also provide opportunities for societal and economic benefits. To supply the trade, wildlife is often sourced from biodiverse developing countries where poverty rates are high. Ensuring a legal and sustainable trade is therefore critical not only for conservation and implementation of the Convention on International Trade in Endangered Species (CITES), but can contribute to UN Sustainable Development Goals to reduce poverty in developing regions. This thesis investigates trade in live animals, with emphasis on socio-economic implications of wildlife trade chains, and how these interact with conservation and sustainable use in supply countries. An interdisciplinary approach utilises global analysis of wildlife trade data; social research methods to examine the trade in Madagascar; and a specialised questioning technique to explore sustainability of the trade at the end-user level. The findings demonstrate an increasing component of the reptile pet trade comprises animals from ranching operations, or captive-bred in consumer countries. Although this may take pressure off wild populations, it may have implications for biodiversity and benefit sharing in supply countries. In Madagascar, a small proportion of the export value of reptiles and amphibians reaches local collectors. Whilst being potentially profitable and providing additional cash income to some households, wildlife trapping is also unreliable, part-time and financially risky. Consequently, it appears to bring limited opportunities for poverty alleviation or incentives for conservation at the local scale. Value chain analysis reveals the informal and complex nature of the supply chain, making design and implementation of interventions to enhance the trade challenging. Findings suggest that initiatives may be most effective working at the local level to improve organisation and cooperative management of the trade. At the consumer end, mortality of pet reptiles varies between taxa but appears to be relatively low. This directly informs debate concerning exotic pet keeping in consumer countries, for which there are limited data concerning sustainability of wildlife supply chains. Together, these studies enhance knowledge regarding implications of the wildlife trade for livelihoods and conservation, and inform dialogue concerning wildlife trade policy and practice more generally.
• Tinoco, M. (2016). Habitat Change and the Status of the Herpetofauna in the Atlantic Forest on the North Coast of Bahia, Brazil.
  Abstract View in KAR
  Conservation priorities are increasingly focused on biodiversity hotspots. As far as amphibians and reptiles are concerned, areas of exceptionally high diversity are centered on tropical and subtropical regions. The Great Desert of Australia, the USA and the Kalahari desert, the Amazon rainforest, and the forests of Thailand are some of the regions sharing the highest biodiversity in the globe. These are all large areas of land containing over 200 herpetofauna species. We investigated herpetofauna diversity, species assemblages distributions, occupancy, detection, survival and body condition on a small portion of the Atlantic forest on the north coast of Bahia, Brazil. This ecosystem, known as "restinga", comprises white sand dunes habitats and covers 450 km2. During four years of sampling we recorded over 23,000 individuals from 224 herpetofauna species on nine sites measuring 25 km2 each, covering nearly half of the of remaining restinga habitats. Amphibians were represented by 89 species (86 anurans; 3 caecilians), reptiles by 135 species (60 snakes, 59 lizards, two caimans; 14 testudines). One single 25 km2 grid cell contained over 105 species alone. This level of diversity represents half of the known species richness described for the state of Bahia, and over 12% of the entire Brazilian herpetofauna. Most reptile assemblages are related to the open sand dune habitats and the amphibian assemblages are related to humid areas or the dense forest patches. Occupancy and detection indices were possible for a large number of species, however a few endemic or endangered species showed very low rates. Equally, 'disturbance adaptors' tended to show high levels of occupancy and detectability, while 'disturbance avoiders' showed the opposite pattern. However, there were also some taxonomic differences, with snakes showing lower levels of detectability than lizards or frogs. Capture Mark Recapture analysis was used to determine estimates of annual survival, which was significantly higher in invasive species. Likewise, invasive species tended to show higher body condition indices than native species, and were better able to exploit disturbed sites. Apparently native and endemic species are suffering from habitat loss and urbanization disturbance caused by the growth of tourism in the region. Unfortunately the network of protected areas are failing to protect this impressive hotspot diversity which is under increasing pressure from development, agriculture and tourism.
• Labisko, J. (2016). Evolutionary Relationships of the Sooglossid Frogs of Seychelles’.
  View in KAR
• Hudson, M. (2016). Conservation Management of the Mountain Chicken Frog.
  Abstract View in KAR
  Global biodiversity is being lost at an unprecedented rate, such that we have entered the sixth mass extinction in the history of the earth with emerging infectious diseases (EID) recognised as an important contributor to this loss. Amphibian chytridiomycosis is an EID that has driven very rapid declines in, or even extinctions of, hundreds of amphibian species. Infectious diseases such as chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), often persist in biological and non-biological reservoirs making them difficult to eradicate. In turn, this makes reintroductions of target species challenging due to the risk of infection. This thesis investigates the critically endangered mountain chicken (Leptodactylus fallax) as a case study of the population impacts of a chytridiomycosis epidemic and to test the effectiveness of strategies to mitigate the effects of the disease. Specifically, this research (1) charts the decline of the mountain chicken on the only two islands on which it exists, and determines the impact on genetic diversity; (2) tests whether anti-fungal treatment can improve the survival of mountain chickens with Bd infection in the wild; (3) examines the role of Bd reservoir species in causing Bd infections of reintroduced mountain chickens; and (4) determines habitat features that are predictors of infection at release sites. Chytridiomycosis drove the mountain chicken to near extinction on Dominica in 2002 and Montserrat in 2009, in one of the fastest recorded vertebrate species declines, leading to a significant loss of genetic diversity. On Montserrat, treating mountain chickens with an anti-fungal drug (itraconazole) during the chytridiomycosis epidemic improved survival rates and reduced Bd infection rates in the short term, but did not provide long-term protection. Although mountain chickens have been driven to near-extinction by Bd infection on Montserrat, the pathogen persists in two sympatric reservoir species which are not impacted by Bd infection, the most prolific of which (Eleutherodactylus johnstonei) displays strong seasonality in Bd infection prevalence and load. Timing mountain chicken reintroduction to occur during the period when tree frog Bd infection was at its lowest was tested to determine the impact on reintroduction success. Multi-state mark-recapture modelling applied post-release showed that optimising the timing of release reduced Bd infection rates and increased survival. Radio-tracking was utilised with geographic profiling to determine that release site water bodies were likely sources of Bd infection in reintroduced mountain chickens. This could inform targeted mitigation of the pathogen and improve future reintroduction success. Where species have been extirpated in the wild, and an irreversible threat such as an EID persists, novel reintroduction strategies are required. These include optimising the timing and conditions of release in order to minimise the impact of the threat along with targeted mitigation measures such as individual level treatments.

Forthcoming

• Buxton, A., Groombridge, J. and Griffiths, R. (2018). Comparison of two Citizen Scientist Methods for Collecting Pond Water Samples for Environmental DNA Studies. Citizen Science: Theory and Practice [Online] 3. Available at: http://dx.doi.org/10.5334/cstp.151.
  Abstract View in KAR
  The use of environmental DNA (eDNA) for the survey of aquatic species offers a wide range of benefits over conventional surveys and has begun to be used by citizen scientists. One advantage of eDNA over conventional survey protocols is the comparative ease with which samples can be collected over a wide geographic area by citizen scientists. However, eDNA collection protocols vary widely between different studies, promoting a need to identify an optimum method. Collection protocols include ethanol precipitation and various filtration methods including those that use electronic vacuum or peristaltic pumps, hand pumps or syringes to capture eDNA on a membrane. We compare the effectiveness of two eDNA collection methods suitable for use by citizen scientists: glass-microfiber syringe filtration and ethanol precipitation. Paired samples of water were analysed for great crested newt (Triturus cristatus) DNA using (1) a laboratory tank experiment using different dilutions of water inoculated with newt DNA; and (2) by sampling naturally colonised ponds. Although syringe filters consistently yielded greater DNA extract concentrations in the tank experiments, this was not the case in samples collected from the field where no difference between the two methods was identified. Clearly, properties within the water – such as algae and particulate matter - can influence the amount of DNA captured by the two methods, so the sampling protocol of choice will depend on the design and goals of the study.