PhD researcher, Manchester Metropolitan University
Informing conservation management of a threatened woodland mammal
As conservationists, we want species or populations to survive and persist long into the future. To achieve this, we monitor populations to observe abundances to identify populations that are at risk of becoming extinct in order to inform conservation practices.
it is also important to understand the ecological mechanisms underlying patterns of their abundance and understand how they disperse between different areas. Species are impacted at the popualtion level by variations in density, predators, food availability and climate. Understanding how populations adapt and change to these variations can provide us with the knowledge to conduct conservation management of these populations to ensure long-term survival in the future. This is difficult for a species such as the hazel dormouse, which is elusive and like to spend most of its active time in dense tree canopies.
Available information on the demographic status of dormice across its range suggests that in continental Europe dormice are relatively common and widespread, however in its northern European range it is considered to be declining and as such is strictly protected. The main driver for this is thought to be habitat reduction and fragmentation, however evidence of causation for this is lacking. My research aims to firstly, investigate the role of climatic variation, identifying important factors that can affect the abundances of dormice. Secondly, I use genetic tools to relate dormouse ecology, biology and physiology with an area known as population genetics. This allows us to understand how genetic diverse populations of dormice are and investigate how related populations or individuals may be to each other. Understanding genetic diversity within a particular species and populations is important because it is variation that allows species to adapt to environmental change and avoid problems associated with inbreeding. This research will hopefully play an important role in our management efforts to prioritise good conservation practices in woodlands that benefit species such as the hazel dormouse.
Abstract: To assess the level and spatial pattern of genetic diversity of the common dormouse, Muscardinus avellanarius, we developed polymorphic microsatellite loci from partial genomic libraries enriched for microsatellite motifs. Ten dinucleotide polymorphic microsatellites were isolated and levels of genetic diversity were assessed in 139 individuals from Bontuchel, (Denbighshire, Wales). We observed high levels of heterozygosity (mean H(O) = 0.792 ± 0.077; mean H(E) = 0.730 ± 0.084) and a large number of alleles (N(a) = 6-17). There was no evidence of deviations from Hardy-Weinberg conditions, or genotypic disequilibrium between any pairs of loci. This is the first description of microsatellite primers from a common dormouse and these loci are currently being used to quantify dormouse spatial genetic structure.
Pub.: 01 May '09, Pinned: 12 Sep '17
Abstract: Mating behaviour is an important component of species’ life histories. Knowledge of natural patterns of mating can lead also to more effective management strategies for populations of conservation concern. Despite a high conservation profile many aspects of the biology of the common dormouse (Muscardinus avellanarius) remain unknown, potentially limiting present conservation efforts. We determine the mating behaviour of M. avellanarius at two woodland sites in the UK: (1) Bontuchel (a natural population in Wales) and (2) Wych (a population in England that was established by reintroducing captive-bred animals) by genotyping mothers and litters at a panel of 10 microsatellite loci. Adult female body weight positively correlates with litter size and no apparent reproductive skew was evident. We found that multiple mating by female dormice is prevalent at both sites, with litters containing three or more offspring sired by multiple fathers; moreover, multiple mating is adopted by released animals even after a period of captive breeding where females are mated singly or as a breeding pair. We also present evidence for low proportion of fathers identified in our samples that probably related to unsampled individuals and/or larger than anticipated population sizes. This first report of mating behaviour in M. avellanarius highlights the role of genetic studies to uncover species’ reproductive behaviours and include these data for conservation management.
Pub.: 13 Mar '11, Pinned: 12 Sep '17
Abstract: Quantitative descriptions of population genetic structure allows the delineation of population units and is therefore of primary importance in population management and wildlife conservation. Yet, predicting factors that influence the gene flow patterns in populations particularly at landscape scales remains a major challenge in evolutionary biology. Here we report a population genetic study of the common dormouse, Muscardinus avellanarius, a species that is seriously threatened due to anthropogenic factors, in two regions, Bontuchel (Denbighshire) and Afonwen (Gwynedd), both in Wales, UK. Ten microsatellite loci were used to characterize patterns of genetic diversity of M. avellanarius within both regions. While the population differentiation between both regions is apparent through geographical scale separating them, by using Bayesian clustering analyses, we identified the occurrence of genetic division among populations of M. avellanarius in Bontuchel region, but no significant evidence of differentiation in Afonwen. We found a strong significant isolation-by-distance (IBD) pattern at a fine-scale (less than 1 km) within continuous habitat and between habitat patches in both regions. Overall, analyses suggest that small-scale dispersal associated with the social structure and dispersal tendencies of this species is reflected in the genetic structure of populations. These findings then provide useful baseline data for supporting local management strategies.
Pub.: 24 May '11, Pinned: 12 Sep '17
Abstract: The common dormouse is a European protected species that is considered at risk during forest management operations in the UK. Historically, they were believed to exist principally in scrub and broadleaved woodlands, especially hazel coppice, but recent evidence has shown that they are present in some conifer sites at low density. Operations to restore conifer plantations on ancient woodland sites (PAWS) with native broadleaves may be especially hazardous to dormice populations, since dormouse densities are generally lower here so sudden perturbations may cause local extinction. Recent policy for restoring PAWS to broadleaved and the need to comply with European legislation has emphasised the need to devise appropriate but pragmatic forest management protocols involving the phased removal of conifers over time. Dormice were handled and individually marked on a single 12 ha conifer PAWS site from 2000 and a density index calculated from 2002 to 2007. In four adjacent study areas, a different form of PAWS restoration was carried out in 2003 to remove c. 33% of conifers. The effects on dormouse numbers, damage to artificial hibernation nests, and regeneration of suitable habitat were recorded. Monitoring indicated that dormouse populations were sustained in each study area after management, suggesting that at this site, conifer removal operations did not have a significant detrimental effect on the dormouse population. Damage to artificial hibernation nests was significantly different between the four study areas. The least damage occurred in the study area containing large group fells due to potential refuge areas, and worst in the traditional standard overall thinning. Measured differences in shrub vegetation throughout each study area showed that numerous small group fells or a few larger group fells subsequently regenerated to form a better vegetation structure for dormice than the traditional standard overall thinning. The implications for forest managers of the results from this single site are discussed.
Pub.: 18 Feb '12, Pinned: 12 Sep '17
Abstract: Hazel dormice, Muscardinus avellanarius (Rodentia: Gliridae) are vulnerable to habitat loss and fragmentation, and thus protected by European Directives. We isolated hazel dormouse microsatellite sequences from enriched genomic libraries to facilitate conservation-focussed research, such as population genetics, regarding this threatened species. Fifty-three primer sets were designed from 51 newly isolated loci. Additionally, we redesigned and tested nine primer sets from previously-published hazel dormouse microsatellite sequences. These 62 marker sets were initially tested in eight unrelated individuals. Thirty-nine loci, which were polymorphic and amplified in >88 % of these samples (extracted from hair), were then genotyped and characterised in 22–26 individuals. Of these, 26 autosomal loci (18 new and eight published) adhered to Hardy–Weinberg equilibrium (p ≤ 0.05) and displayed an estimated null allele frequency of <0.10. One loci pair displayed linkage disequilibrium after correction for multiple tests.
Pub.: 02 Apr '13, Pinned: 12 Sep '17
Abstract: Movement is an important life history trait that can have an impact on local adaptation, and other evolutionary phenomena. We used a combination of nestbox survey data and genetic techniques (genotyping at 10 microsatellite loci) to quantify patterns of movement in common dormice Muscardinus avellanarius at two distinct sites in the UK: 1) Bontuchel (a natural population) and 2) Wych (captive-bred individuals that were reintroduced to this site), over three consecutive years (2006-2008). Both methods revealed a consistent pattern of sex-biased movement (movements by adult males and females) in both populations that allowed isolation-by-distance genetic structure to develop within 1 km. The similarity of data from captive-bred and natural individuals indicated that ex situ programing has not significantly altered the natural movement behavior of common dormice; consequently, the two populations could be managed with the same conservation strategies. We also found that the reintroduced dormice in Wych maintained relatively high levels of genetic diversity. This first report of movement patterns in reintroduced and natural populations of M. avellanarius combining genetic and field-survey data highlights the role of genetic studies in the investigation of ecological behaviour and for conservation management.
Pub.: 22 Jan '14, Pinned: 12 Sep '17
Abstract: We studied the effect of a forest edge management quasi-experiment on hazel dormouse (Muscardinus avellanarius) nest numbers in the reproductive season in the Netherlands. We found that the number of nests increased significantly from 2009 to 2013 in managed edges after clearing 75–100 % of mature trees, with a peak in the second year, whereas those in unmanaged edges decreased. In addition, we studied habitat characteristics in forest edges and hedgerows, and found a positive effect of a high upper shrub layer and a high abundance of blackberry (Rubus fruticosus agg. and Rubus spp.), rowan (Sorbus aucuparia) and common hawthorn (Crataegus monogyna) on nest densities. Based on these results, we propose a potential dormouse management strategy that extends conventionally advocated coppice management for regions with well-developed forest edges by (i) postulating a blackberry-oriented landscape restoration approach and (ii) using clearing of mature trees as a tool to boost local dormouse populations in forest edges that have become unsuitable as dormouse habitat due to vegetational succession.
Pub.: 07 Aug '14, Pinned: 12 Sep '17
Abstract: The success of any population translocation programme relies heavily on the measures implemented to control and monitor the spread of disease. Without these measures, programmes run the risk of releasing immunologically naïve species or, more dangerously, introducing novel infectious agents to native populations. As a precaution, a reintroduction programme for the common or hazel dormouse, Muscardinus avellanarius, in England screens dormice before release following captive breeding. Using PCR sequencing of a range of genes, we tested whether the same species of tapeworm(s) were present in captive and free-living dormice. Whilst only Rodentolepis straminea were identified in free-living dormice, cestode ova found in a captive individual produced a molecular match closely related to Hymenolepis microstoma and a previously unrecorded Rodentolepis species. To prevent putting at risk the free-living population, we recommended the continued treatment of dormice showing tapeworm infection before release. Our work demonstrates how molecular techniques can be used to inform reintroduction programmes, reduce risk from disease and increase chances of reintroduction success.
Pub.: 08 Mar '16, Pinned: 12 Sep '17
Abstract: Yearly variations in the diet composition of the hazel dormouse Muscardinus avellanarius were studied in typical dormouse habitat in Lithuania over 5 years (2010–2014) with different feeding conditions. A high proportion of birch seeds in the dormouse diet in two out of 5 years was a very much unexpected result. Dormice consumed them from mid-June until late October even when the most preferable food—hazel nuts—was abundant. In autumn when accumulating fat reserves for hibernation, hazel dormice fed on four main food sources—fruits of glossy buckthorn, oak acorns, hazel nuts and birch seeds. The consumption of these food sources was directly related to their availability. During the study period, only one, two or three of these food sources were abundant in any particular year, while others were absent or scarce. In total, the fruits of glossy buckthorn and oak acorns accounted for the major portion of dormouse diet in autumn. Dormice living in habitat with irregular fruiting of the main food plants are adapted to feed on varying food sources and can switch from one food source to another in different years.
Pub.: 18 May '16, Pinned: 12 Sep '17
Abstract: Habitat fragmentation hinders the dispersal process, which, in turn, causes changes to the genetic variability of populations. The aim of this study was to evaluate the effects of fragmentation on the genetic population features of the hazel dormouse (Muscardinus avellanarius), a small rodent living in forest habitats, using seven microsatellite loci. We compared (i) the genetic variability and population structure, (ii) the scale of the spatial structuring, and (iii) the possible presence and effect of a sex-biased dispersal in two populations living, respectively, in a continuous and in a fragmented landscape in central Italy. Although all microsatellite loci were always polymorphic, in the fragmented population the observed heterozygosity was usually lower than expected, and 5 out of 7 loci were not at Hardy–Weinberg Equilibrium. The fragmented population was found to be strongly structured. These results showed that there was a hindrance of the gene flow between subpopulations, and in some cases even a virtual ecological isolation, as confirmed by the absence of covariation between the pairwise genetic and Euclidean distances. Some clues of female-biased dispersal were found, but even the dispersing sex showed dispersal problems in several cases. The strong differences in the genetic features between the continuous and fragmented population, indicate that the hazel dormouse strongly suffers from habitat fragmentation. This happens even when several neighbouring habitats remnants persist and remain partially connected by verges along crop fields. Thus, the fragmented landscape needs urgent measures to restore ecological connectivity through a more effective management plan of the hedgerows network.
Pub.: 21 Oct '16, Pinned: 12 Sep '17
Abstract: Populations of many species show temporally synchronous dynamics over some range, mostly caused by spatial autocorrelation of the environment that affects demographic rates. Synchronous fluctuation of a demographic rate is a necessary, but not sufficient condition for population synchrony because population growth is differentially sensitive to variation in demographic rates. Little is known about the relative effects of demographic rates to population synchrony, because it is rare that all demographic rates from several populations are known. We develop a hierarchical integrated population model with which all relevant demographic rates from all study populations can be estimated and apply it to demographic data of barn swallows Hirundo rustica from nine sites that were between 19 and 224 km apart from each other. We decompose the variation of the population growth and of the demographic rates (apparent survival, components of productivity, immigration) into global and local temporal components using random effects which allowed the estimation of synchrony of these rates. The barn swallow populations fluctuated synchronously, but less so than most demographic rates. The highest synchrony showed the probability of double brooding, while fledging success was highly asynchronous. Apparent survival, immigration and total productivity achieved intermediate levels of synchrony. The growth of all populations was most sensitive to changes in immigration and adult apparent survival, and both of them contributed to the observed temporal variation of population growth rates. Using a simulation model, we show that immigration and apparent survival of juveniles and adults were able to induce population synchrony, but not components of local productivity due to their low population growth rate sensitivity. Immigrants are mostly first-time breeders, and consequently, their number depends on the productivity of neighbouring populations. Since total productivity was synchronized, we conclude that it contributed to population synchrony in an indirect way through dispersing individuals which appear as immigrants at the local scale. The hierarchical integrated population model is promising for achieving an improved mechanistic understanding of population synchrony.
Pub.: 17 Jul '15, Pinned: 12 Sep '17
Abstract: Discrete state‐space models are used in ecology to describe the dynamics of wild animal populations, with parameters, such as the probability of survival, being of ecological interest. For a particular parametrization of a model it is not always clear which parameters can be estimated. This inability to estimate all parameters is known as parameter redundancy or a model is described as nonidentifiable. In this paper we develop methods that can be used to detect parameter redundancy in discrete state‐space models. An exhaustive summary is a combination of parameters that fully specify a model. To use general methods for detecting parameter redundancy a suitable exhaustive summary is required. This paper proposes two methods for the derivation of an exhaustive summary for discrete state‐space models using discrete analogues of methods for continuous state‐space models. We also demonstrate that combining multiple data sets, through the use of an integrated population model, may result in a model in which all parameters are estimable, even though models fitted to the separate data sets may be parameter redundant.
Pub.: 30 Jun '16, Pinned: 12 Sep '17
Abstract: Understanding the ecological processes that are involved in the transmission of zoonotic pathogens by small mammals may aid adequate and effective management measures. Few attempts have been made to analyze the ecological aspects that influence pathogen infection in small mammals in livestock production systems. We describe the infection of small mammals with Leptospira spp., Brucella spp., Trichinella spp. and Cysticercus fasciolaris and assess the related intrinsic and extrinsic factors in livestock production systems in central Argentina at the small mammal community, population and individual levels.Ten pig farms and eight dairy farms were studied by removal trapping of small mammals from 2008 to 2011. Each farm was sampled seasonally over the course of one year with cage and Sherman live traps. The 505 small mammals captured (14,359 trap-nights) included three introduced murine rodents, four native rodents and two opossums. Leptospira spp., anti-Brucella spp. antibodies and Trichinella spp. were found in the three murine rodents and both opossums. Rattus norvegicus was also infected with C. fasciolaris; Akodon azarae and Oligoryzomys flavescens with Leptospira spp.; anti-Brucella spp. antibodies were found in A. azarae. Two or more pathogens occurred simultaneously on 89% of the farms, and each pathogen was found on at least 50% of the farms. Pathogen infections increased with host abundance. Infection by Leptospira spp. also increased with precipitation and during warm seasons. The occurrence of anti-Brucella spp. antibodies was higher on dairy farms and during the winter and summer. The host abundances limit values, from which farms are expected to be free of the studied pathogens, are reported.Murine rodents maintain pathogens within farms, whereas other native species are likely dispersing pathogens among farms. Hence, we recommend preventing and controlling murines in farm dwellings and isolating farms from their surroundings to avoid contact with other wild mammals.
Pub.: 01 Jul '17, Pinned: 12 Sep '17
Abstract: Abstract Robust identification of species and significant evolutionary units (ESUs) is essential to implement appropriate conservation strategies for endangered species. However, definitions of species or ESUs are numerous and sometimes controversial, which might lead to biased conclusions, with serious consequences for the management of endangered species. The hazel dormouse, an arboreal rodent of conservation concern throughout Europe is an ideal model species to investigate the relevance of species identification for conservation purposes. This species is a member of the Gliridae family, which is protected in Europe and seriously threatened in the northern part of its range. We assessed the extent of genetic subdivision in the hazel dormouse by sequencing one mitochondrial gene (cytb) and two nuclear genes (BFIBR, APOB) and genotyping 10 autosomal microsatellites. These data were analysed using a combination of phylogenetic analyses and species delimitation methods. Multilocus analyses revealed the presence of two genetically distinct lineages (approximately 11 % cytb genetic divergence, no nuclear alleles shared) for the hazel dormouse in Europe, which presumably diverged during the Late Miocene. The phylogenetic patterns suggests that Muscardinus avellanarius populations could be split into two cryptic species respectively distributed in western and central-eastern Europe and Anatolia. However, the comparison of several species definitions and methods estimated the number of species between 1 and 10. Our results revealed the difficulty in choosing and applying an appropriate criterion and markers to identify species and highlight the fact that consensus guidelines are essential for species delimitation in the future. In addition, this study contributes to a better knowledge about the evolutionary history of the species.AbstractRobust identification of species and significant evolutionary units (ESUs) is essential to implement appropriate conservation strategies for endangered species. However, definitions of species or ESUs are numerous and sometimes controversial, which might lead to biased conclusions, with serious consequences for the management of endangered species. The hazel dormouse, an arboreal rodent of conservation concern throughout Europe is an ideal model species to investigate the relevance of species identification for conservation purposes. This species is a member of the Gliridae family, which is protected in Europe and seriously threatened in the northern part of its range. We assessed the extent of genetic subdivision in the hazel dormouse by sequencing one mitochondrial gene (cytb) and two nuclear genes (BFIBR, APOB) and genotyping 10 autosomal microsatellites. These data were analysed using a combination of phylogenetic analyses and species delimitation methods. Multilocus analyses revealed the presence of two genetically distinct lineages (approximately 11 % cytb genetic divergence, no nuclear alleles shared) for the hazel dormouse in Europe, which presumably diverged during the Late Miocene. The phylogenetic patterns suggests that Muscardinus avellanarius populations could be split into two cryptic species respectively distributed in western and central-eastern Europe and Anatolia. However, the comparison of several species definitions and methods estimated the number of species between 1 and 10. Our results revealed the difficulty in choosing and applying an appropriate criterion and markers to identify species and highlight the fact that consensus guidelines are essential for species delimitation in the future. In addition, this study contributes to a better knowledge about the evolutionary history of the species.bbMuscardinus avellanarius
Pub.: 08 Oct '16, Pinned: 14 Aug '17
Abstract: Within the framework of landscape genetics, resistance surface modelling is particularly relevant to explicitly test competing hypotheses about landscape effects on gene flow. To investigate how fragmentation of tropical forest affects population connectivity in a forest-specialist bird species, we optimized resistance surfaces without a priori specification, using least-cost (LCP) or resistance (IBR) distances. We implemented a two-step procedure in order i) to objectively define the landscape thematic resolution (level of detail in classification scheme to describe landscape variables) and spatial extent (area within the landscape boundaries) and then ii) to test the relative role of several landscape features (elevation, roads, land cover) in genetic differentiation in the Plumbeous Warbler (Setophaga plumbea). We detected a small-scale reduction of gene flow mainly driven by land cover, with a negative impact of the non-forest matrix on landscape functional connectivity. However, matrix components did not equally constrain gene flow, as their conductivity increased with increasing structural similarity with forest habitat: urban areas and meadows had the highest resistance values whereas agricultural areas had intermediate resistance values. Our results revealed a higher performance of IBR compared to LCP in explaining gene flow, reflecting sub-optimal movements across this human-modified landscape, challenging the common use of LCP to design habitat corridors and advocating for a broader use of circuit theory modelling. Finally, our results emphasize the need for an objective definition of landscape scales (landscape extent and thematic resolution) and highlight potential pitfalls associated with parameterization of resistance surfaces. This article is protected by copyright. All rights reserved.
Pub.: 21 Jul '17, Pinned: 14 Aug '17
Abstract: Torpor is thought to slow age-related processes and to sustain growth and fattening of young individuals. Energy allocation into these processes represents a challenge for juveniles, especially for those born late in the season. We tested the hypothesis that late-born juvenile garden dormice (Eliomys quercinus) fed ad libitum ('AL', n = 9) or intermittently fasted ('IF', n = 9) use short torpor bouts to enhance growth and fat accumulation to survive winter. IF juveniles displayed more frequent and longer torpor bouts, compared with AL individuals before hibernation. Torpor frequency correlated negatively with energy expenditure and water turnover. Hence, IF juveniles gained mass at the same rate, reached similar pre-hibernation fattening and displayed identical hibernating patterns and mass losses as AL animals. We found no group differences in relative telomere length (RTL), an indicator of ageing, during the period of highest summer mass gain, despite greater torpor use by IF juveniles. Percentage change in RTL was negatively associated with mean and total euthermic durations among all individuals during hibernation. We conclude that torpor use promotes fattening in late-born juvenile dormice prior to hibernation. Furthermore, we provided the first evidence for a functional link between time spent in euthermy and ageing processes over winter.
Pub.: 08 Nov '14, Pinned: 14 Aug '17
Abstract: The development of appropriate wildlife survey techniques is essential to promote effective and efficient monitoring of species of conservation concern. Here, we demonstrate the utility of two rapid-assessment, non-invasive methods to detect the presence of elusive, small, arboreal animals. We use the hazel dormouse, Muscardinus avellanarius, a rodent of conservation concern, as our focal species. Prevailing hazel dormouse survey methods are prolonged (often taking months to years to detect dormice), dependent on season and habitat, and/or have low detection rates. Alternatives would be of great use to ecologists who undertake dormouse surveys, especially those assessing the need for mitigation measures, as legally required for building development projects. Camera traps and footprint tracking are well-established tools for monitoring elusive large terrestrial mammals, but are rarely used for small species such as rodents, or in arboreal habitats. In trials of these adapted methods, hazel dormice visited bait stations and were successfully detected by both camera traps and tracking equipment at each of two woodland study sites, within days to weeks of installation. Camera trap images and footprints were of adequate quality to allow discrimination between two sympatric small mammal species (hazel dormouse and wood mouse, Apodemus sylvaticus). We discuss the relative merits of these methods with respect to research aims, funds, time available and habitat.
Pub.: 21 Jan '16, Pinned: 14 Aug '17
Abstract: Along with the periodic reductions in O2 requirements of mammalian hibernators during winter, the O2 affinity of the blood of mammalian hibernators is seasonally regulated to help match O2 supply to consumption, contributing to limit tissue oxidative stress, particularly at arousals. Specifically, mammalian hibernators consistently show an overall increase in the blood-O2 affinity, which causes a decreased O2 unloading to tissues, while having similar or lower tissue O2 tensions during hibernation. This overview explores how the decreased body temperature and concentration of red blood cell 2,3-diphosphoglycerate (DPG) that occur in hibernation contribute separately or in combination to the concurrent increase in the O2 affinity of the hemoglobin, the O2 carrier protein of the blood. Most mammalian hemoglobins are responsive to changes in DPG concentrations, including that of the hibernating brown bear, although the smaller hibernators, such as golden-mantled ground squirrel, chipmunks, and dormice, have hemoglobins with low sensitivity to DPG. While the effect of DPG on oxygenation may vary, the decrease in body temperature invariably increases hemoglobin's O2 affinity in all hibernating species. However, the temperature sensitivity of hemoglobin oxygenation is low in hibernators compared to human, apparently due in part to endothermic allosteric quaternary transition in ground squirrels and dissociation of chloride ions in brown bears. A low heat of blood oxygenation in temporal heterotherms, like hibernators, may thus contribute to reduce heat loss, as found in regional heterotherms, like polar mammals, although the significance would be low in winter hibernation.
Pub.: 23 Mar '17, Pinned: 14 Aug '17