The Origins of the Co. Kildare Dormouse

Deborah G. Glass1, Dawn M. Scott1, Daniel Donoher2, Andrew D.J. Overall1

1Division of Biology, University of Brighton, Brighton, BN2 4GJ, UK. Corre-

sponding author email: D.Glass2@brighton.ac.uk.

2Kildare Animal Foundation, South Green Road, Kildare Town, County Kildare.

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ABSTRACT

The Hazel dormouse Muscardinus avellanarius has recently been discovered in

Co. Kildare Ireland and is being treated as non-native and, hence, potentially inva-

sive. The mode of arrival and origins are unknown, initial theories included transferal

via hay from Great Britain. The population in Kildare appears to be thriving and

as native populations throughout England are in decline, the success is of broad con-

servation relevance. To gain insight into the recent demography of the Co. Kildare

population, the cytochrome b gene was profiled for individuals from Kildare, Eng-

land and Wales and compared to known haplotypes throughout its European range.

The individuals from Co. Kildare shared the same previously unrecorded haplo-

type, which was placed in a separate clade from the GB haplotype, along with more

southern European populations. The French haplotype was the most recent common

ancestor, albeit with a 3 base pair di↵erence. Inferring either the dormouse has been

present in Ireland for longer than expected, or is derived from a recent source pop-

ulation yet to be sampled. The latter is considered the most likely scenario. Future

work and concerns of the Hazel dormouse in Ireland are discussed.

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1 Introduction

The hazel dormouse Muscardinus avellanarius has recently been observed in Ireland,

with the first reported sighting located within County Kildare in 2010 (Marnell et al,

2013). How the dormouse arrived in Ireland and from where it derived is currently

unknown. Muscardinus avellanarius is otherwise distributed widely across Europe,

from the Mediterranean to Southern Sweden and eastwards towards Russia, but ex-

cluding Iberia. The range also extends to parts of Asia Minor (Juskaitis, 2007). The

northwest limit of its European range is in Great Britain (GB), where it is found

over much of Southern England, with some isolated populations in northern Wales

(Bright et al. 2006). In parts of its Northern range (UK, Netherlands, Sweden,

Germany and Denmark) populations are declining; as a consequence they are pro-

tected under the European Habitats directive annex IV and the Bern convention

Appendix III (ICUN 2014). There are no historical records of the presence of the

dormouse in Ireland; hence they are considered as non-native and potentially inva-

sive. In addition, Invasive species are recognised as an important element in global

change (Occhipinti-Ambrogi 2007), therefore it is important to closely monitor any

non-native species within their new environment.

Mainland Britain and Ireland have strikingly di↵erent biota, despite being neigh-

bouring islands (Martınkora et al, 2007; McDevitt et al, 2011). Britains flora and

fauna is broadly similar to nearby areas of continental Europe, although it is some-

what restricted (Martınkora et al, 2007). The distinctness between Irish and British

fauna is particularly clear in mammals (Yalden 1999). Native small mammal species

of mainland Britain consist of: four mouse species, four vole species, four shrew

species, one squirrel species and the hazel dormouse (Yalden 1999; Masceretti et al,

2003). Ireland in comparison is species poor, with only five small mammal species

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in total, the pygmy shrew, the woodmouse, the bank vole, the greater white-toothed

shrew and the red squirrels (Yalden 1999; Masceretti et al, 2003; Martınkora et al,

2007; McDevitt et al, 2011; Montgomery et al, 2011). Although it is extremely

di�cult to establish the status of mammals in Ireland perceived as native, due to

uncertainties of natural reinvaders after the last glaciation (Montgomery et al, 2011),

the pygmy shrew, the woodmouse and the red squirrel are considered to be native

and the rest recent invaders (Yalden 1999; Martınkora et al, 2007; McDevitt et al,

2011; Montgomery et al, 2011).

Whether intentional or accidental, the means of introduction is uncertain. Initial

theories of potential arrival routes include the transfer of individuals via hay, through

the horticultural trade and horse racing industry (Marnell et al, 2013). The extensive

horse-breeding and racing industry, in Co. Kildare results in the regular tra�c of

horse boxes back and forth throughout GB (ibid). There have been further possible

sightings in a number of locations including, Dublin, Laois, Tipperary, Clare, Galway,

Mayo, Kerry and Westmeath (Mooney 2013; Sheehy & Lawton, 2014), although

the only confirmed sightings are of 14 individuals within a 29.6 km2 area of the

Newbridge/Naas region of Co. Kildare (Sheehy & Lawton, 2014).

The hazel dormouse is a nocturnal, arboreal mammal that mainly inhabits areas

of deciduous forest with a thick layer of underbrush, although it has been found in

mixed deciduous-coniferous forests and in hedgerows (Bright et al. 2006). The shy,

arboreal and nocturnal nature of the hazel dormouse in addition to their typically

low population density, makes them notoriously di�cult to observe in their native

range (Bright & Morris 1996; Bright et al. 2006, Naim et al. 2011), thus it may

be possible that the species has been present in the Republic of Ireland for longer

than records indicate. The earliest historical record is of an attempted introduction

by the well-known Irish naturalist R.M. Barrington, who tried to introduce six hazel

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dormice, sourced from London, into Fassaroe, Co. Wicklow in 1885. However, no

further evidence of them was recorded and it has since been assumed that they failed

to become established (Fitter 1959).

Given that the native populations throughout England are in decline, some appre-

ciation of the apparent recent success of the Irish dormouse is of broad conservation

relevance. To this end it was considered necessary to establish what the current ge-

netic diversity of the Kildare population is, which o↵ers some indication of the small-

est size of the common ancestral population the e↵ective population size. This, in

turn provides some indication of whether the current population has grown up from

few (single introductory event) or many (multiple independent introductions). Ge-

netic profiling involved the analysis of a single variable region of the mitochondrial

DNA, the cytochrome b region, which has been profiled for hazel dormouse popu-

lations across their European range (Mouton et al, 2012). Mutational di↵erences

between cytochrome b haplotypes are understood to correlate with time since they

shared a recent ancestry (Avise, 2004). Consequently, similarity of haplotypes is

expected to identify the most likely source population.

2 Materials & Methods

2.1 Sample Collection

Samples were collected from Kildare, Ireland; from Sussex, the Isle of Wight and

South Devon, England and from north Wales (see table 1). All tissue samples were

provided from animals which died of natural causes. Those from the UK were col-

lected by volunteers involved with the dormouse monitoring scheme (see acknowl-

edgments). The GB hair samples were collected under a Natural England licence by

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the authors. Hair and tissue samples from the Kildare individuals were provided by

Kildare Animal Foundation, Kildare, Ireland.

DNA was extracted from tissue (ear or tail) samples using the DNeasy Tissue

Kit (QIAGEN) following the manufacturers instructions. Hair sample extraction

required an initial digestion step to maximise DNA yield, following the protocol

by Pfie↵er et al. (2004), before continuing with the DNeasy Kit. A master mix

containing 182.6µl of PCR grade water, 34µl of Tris-HCL (100mM), 34µl of sodium

chloride (100mM), 1.02µl of calcium chloride (3mM), 68µl of 10% SDS, 13.6µl of

40mM DTT and 6.8µl of 250µg/ml Protienase K per sample was added to a 2ml

Eppendorf tube and vortexed for 30 seconds. Each hair sample (>10 hairs with

visible root) was placed in a 1.5ml Eppendorf tube, to which 340µl of the extraction

solution was added and voretexed for 5 seconds. The sample was then transferred to

a water bath set at 56 �C and left to incubate for 2 hours (or until the sample was

fully dissolved), vortexting every half hour. Once the hair was dissolved, the DNeasy

Tissue Kit was used from step 3 of the manufacturers instructions.

2.2 Mitochondrial DNA Analysis

In order to locate the most likely source population for the Kildare dormouse, we

utilized a recent study by Mouton et al, (2012) that provided sequence data from

a 704 base pair (bp) region of the cytochrome b gene. This study identified 33

haplotypes located throughout the M. avellanarius range, excluding Britain. New

sequences were obtained from the Kildare, English and Welsh populations, the latter

two such that the nearest geographical neighbours to Ireland were included in the

analysis.

Table 1

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Table 1 Geographic locations, corresponding lineages and Genbank accession num-

bers of GB and Irish haplotypes.

A 704 bp fragment of the cytochrome b region of the mtDNA was amplified by

PCR using primers: LMA14255, 5-TGGTGGAATTTCGGTTCTCT 3; RMA15192,

5- GTTGCCTCCAATTCATGTT-3 (Mouton et al, 2012). Amplifications were car-

ried out in 25µl reactions containing 5ng of DNA template and final concentrations

of 15nM 10 x reaction bu↵er, 1.5mM MgCl2, 0.2mM for each dNTP, 10 pmol forward

and reverse primers, 1unit PlatinumTaq DNA polymerase (Invitrogen). Cycling was

performed in Techne TC-4000 Thermal cycler employing 40 cycles (30-45 s at 94 �C,

30 45 s at 50 �C and 45-90 s at 72 �C), with a final extension at 72 �C for 10 minutes.

Sequencing procedures were performed by SourceBioscience (Nottingham, England).

MEGA 6 (Tamura et al, 2013) software was employed to generate sequence align-

ments and pairwise genetic distances. MrBayes (version 3.2.2, Ronquist et al, 2012)

was used to construct Bayesian Markov chain Monte Carlo (MCMC) phylogenetic

trees in order to establish the evolutionary relationships among all haplotypes, for

which we ran 50,000 generations, but otherwise the default priors. The garden dor-

mouse (Eliomys quercinus) and edible dormouse (Glis glis) were used as out-groups,

in keeping with the Mouton et al, (2012) study and the Gliridae molecular phy-

logeny (Montgelard et al, 2003). Minimum spanning networks were generated using

Arlequin (ver. 3.5, Exco�er et al, 2005) to calculate connection values, which were

then input into HapStar (Teacher & Gri�ths, 2011).

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3 Results

All six individuals from Kildare, Ireland, had identical cytochrome b sequences (Gen-

bank accession number KJ631620). A Nucleotide BLAST search (NCBI) found the

closest match to be haplotype 20 (assession number FN796772), which relates to

the Mouton et al, (2012) French sample. All individuals sampled throughout GB

had identical haplotypes, identical to Polish haplotype 15 within the Central North

Europe lineage (Lithuania, Poland, Germany). A consensus haplotype, GB 15, is

included in the phylogenetic tree to highlight the genetic distance between the geo-

graphic neighbours, GB and Ireland (Fig 1). The phylogenetic analysis placed the

Irish haplotype within Western Europe lineage containing haplotypes from France,

Belgium and Switzerland. The Irish haplotype was 3 mutational steps from the

French haplotype 20 (Fig 1(b)).

Figure 1

Figure 1 (a) Bayesian phylogenetic analysis of Cytochrome b haplotypes of Mus-

cardinus avellanarius, including those from Mouton et al, (2012) and including sup-

port values. Geographic origins are followed by haplotype number. (b) Detail of

minimum spanning network corresponding to the mutational steps between haplo-

types. The dotted lines connect to the remainder of the network, which is identical

to Figure 3 in Mouton et al, (2012).

Genetic distances (table 2) show the Irish haplotype to have the greatest similarity

to the French (0.4%). The genetic distances between the Irish and the Central

Italian and Central - North Europe lineages is considerably higher at 3.9% and 9.5%

respectively.

Table 2

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Table 2 Cytochrome b genetic distance (%).

4 Discussion

Phylogenetic analysis of the cytochrome b region of the mtDNA produced a number

of revelations. Firstly, the Kildare population shares a recent common ancestry

amongst the Western Europe lineage, whereas the GB population clusters amongst

the Central - North Europe lineage. Our Bayesian tree topology (Fig 1(a)) is identical

to that of Mouton et al, (2012), although our minimum spanning network (Fig 1(b))

connects the Western Europe lineage to the Central Europe lineage via Belgium,

as opposed to the Swiss haplotype 19; otherwise the network is identical to that of

Mouton et al, (2012). The Irish haplotype di↵ers from its closest relative, the French,

at three nucleotide sites. This could suggest that the dormice have been established

in Ireland for a long enough period to accrue this degree of divergence from its closest

neighbours. But, given the lack of observational data, this seems highly unlikely. In

addition, a recent survey study concluded that, based upon dispersal distances, the

hazel dormouse has probably been present for just seven year - since 2007 (Sheehy

& Lawton, 2014). The unique haplotype means that the specific source population

remains unresolved for the time being. However, the phylogenetic analysis places

it amongst the more western, mainland, European populations. The initial theory

that the dormice entered Kildare through bale transport from GB is looking unlikely,

due to the fact that the GB haplotype was so diverse with 68 nucleotide di↵erences.

Lack of di↵erentiation amongst the GB samples (Welsh, South west, South and South

East), makes it unlikely that the source population is from an unsampled region from

GB. Hay importation from other European countries, particularly those of the south

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and west, may provide the route of entry, but this remains to be established.

Further sampling will be necessary in order to ascertain with less uncertainty the

number of entries into the country. As just six samples from the Irish population

have been sequenced, it would be prudent not to overstate the results. Although

a single founding population from Western Europe is currently supported, further

data may modify this conclusion.

4.1 Future concerns for the hazel dormouse

Our current understanding of the ecology of the hazel dormouse suggests that a

rapid spread throughout Ireland is an unlikely scenario. Muscardinus avellanarius

individuals generally do not disperse very far (Bright & Morris 1991, Bright & Morris

1992, Juskaitis, 2008) and are reluctant to cross open ground (Bright & Morris 1991,

Bright & Morris 1992) and corridor gaps (Bright 1998). Rare inter-patch movement

over 1km has been recorded using genetic techniques (Naim et al, 2011), showing

the occasional long distance movement. Habitat corridor use (such as hedgerows)

is widely recognised to facilitate movement and dispersal between habitat patches

(Baum et al, 2004). Thus, it may be possible that such corridors have facilitated

dormouse dispersal throughout Kildare. Recent sighting-surveys have estimated a

presence in this region for at least seven years (Sheehy & Lawson, 2014).

All information on M. avellanarius comes from their native range, thus it is possi-

ble that the environment within Ireland could give them some competitive advantage

that allows them to be extremely successful in their recipient community. It has been

suggested that the subtle di↵erences between the Irish and British hedgerows may

be responsible for the suggested rapid spread of the dormouse, possibly resulting in

faster breeding than within their native range (Mooney 2013).

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Invasive species are often defined as those that have an adverse e↵ect on their

recipient community. Life history traits of non-native species are crucial factors in

determining a species ability to become invasive in new environments (Osman &

Whitlatch 2007; Alcarlo et al, 2008). The reproductive biology of invasive species

is often characterised by high fecundity, more than one generation a year, and flex-

ible life history events (Alcarlo et al, 2008). Given the recognised characteristics

of invasive species, M. avellanarius is unlikely to become a pest in Ireland. The

hazel dormouse has a relatively low reproductive output compared to other rodent

species, with a maximum of two broods per year (only occurring when conditions

are optimal), and an average of 2-4 juveniles in each litter within their native range

(Juskaitis 2008). Climate is the main limiting factor of hazel dormice populations.

Hibernation through the winter months (Bright et al, 1996) is essential to their sur-

vival, limiting the time period in which they can reproduce. The need to reach

optimal weights before breeding and hibernation (Juskaitis 2008) combined with use

of torpor during adverse weather conditions (cold and wet) (Bright et al, 1996), fur-

ther restricts the time in which they can forage and breed. Even with the possibility

of a higher food supply in the areas they have been introduced, the climate in Ire-

land is similar to areas in GB. With climate and weather as a limiting factor to the

flexibility of M. avellanarius life history events, a population explosion in Ireland

would be unlikely. However, it is possible that the hazel dormouse could impact neg-

atively on the recipient community through interspecific interactions. Inavasional

meltdown is the process by which the invasion of one non-native species is facilated

by another non-native species, compounding their independant impacts on native

species, communities and ecosystems (Montgomery et al, 2011). This has already

been demonstrated in small mammal communities in Ireland. Montgomery et al,

(2011) found bank vole abundance (first invader) to be positively influenced by the

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presence of the greater white-toothed shrew (second invader). They also found that

the greater white-toothed shrew had negative and compounding e↵ects on the abun-

dance of wood mice and the occurrence of pygmy shrews (both considered native

species). However, the rapid rate of expansion of the greater white-toothed shrew

over the past seven years is thought to be partly through human-assisted dispersal

(McDevitt et al., 2014), whereas the hazel dormouse is not associated with humans.

Monitoring the dispersal and growth of hazel dormouse over the next few years, even

if a negative impact is unexpected, is going to be crucial in o↵ering a glimpse of the

likelihood of expansion and possibility of interaction with native communities.

AcknowledgmentsWe would like to thank Jen Bousfield, Adam Grogan, Laurie

Jackson, Jenny Macpherson, Stephen Robinson, Janet Rose and Ian White for their

help in collecting samples.

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                 Figure  1    

                   

       Table  1        Geographic  Origin         Lineage     Number   Haplotype     Genbank                 of  animals       accession    Great  Britain,  South  East  England  (Sussex)   Central  Northern   15   15     FN796767*  Great  Britain,  Southern  England  (Isle  of  Wight)   Central  Northern   5   15  Great  Britain,  South  West  England  (Devon)   Central  Northern   2   15  Great  Britain,  North  Wales  (Carmarthen)     Central  Northern   1   15  Ireland,  Co.  Kildare         Western     6   34     KJ631620    *  From  Mouton  et  al,  (2012)        Table  2               Ireland_34   France_20     Belgium_21   Switz_19   Italy_23                            France_20     0.4  Belgium_21   0.5     0.1  Switz_19     0.5     0.1     0.3  Italy_23     3.9     3.8     3.9     3.6  Germany_14   9.5     9.3     9.2     9.2   9.8