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1
Endoparasites of the endemic Irish hare Lepus timidus hibernicus
SamanthaBall, Thomas C. Kelly and FidelmaButler
S. Ball (https://orcid.org/0000-0002-5147-7111) ✉ (samantha.ball@ucc.ie) T. C. Kelly and F. Butler (https://orcid.org/0000-0001-9256-
3246), School of Biological, Earth and Environmental Science, Distillery Fields, Univ. College Cork, Cork, T23 TK30, Ireland. SB and TK also
at: Dublin Airport Authority, Airport Fire and Rescue Service, Dublin, K67 CX65, Ireland.
e Irish hare Lepus timidus hibernicus is an endemic subspecies of Mountain hare and Ireland’s only native lagomorph.
e endoparasite community composition of the Irish hare was examined from 22 carcasses opportunistically sourced from
wildlife strike events (with aircraft and vehicles) from three counties in the Republic of Ireland. ree parasite taxa were
identied from the stomach and small intestines: Trichostrongylus retortaeformis, Graphidium strigosum and a tapeworm
belonging to the genus Mosgovoyia. Overall, 50% of hares examined were host to at least one endoparasite taxon and 18%
were host to more than one taxon. ere was no signicant correlation between parasite burden and host weight. is is
the rst known study of endoparasites in the Irish hare.
Keywords: ecology, gastrointestinal helminths, Ireland, mountain hare
e Irish hare Lepus timidus hibernicus is a distinct endemic
subspecies of the mountain hare Lepus timidus which is an
ecologically and economically important game species across
its range. While mountain hares are generally arctic–boreal
in range, the Irish hare is an exception, inhabiting a temper-
ate environment (Hamilletal. 2006) and numerous habi-
tat types within Ireland (Lysaght and Marnell 2016). Irish
hare populations have undergone rapid population declines
(Dingerkus and Montgomery 2002, Reidetal. 2010a) and
are now considered a priority species for conservation action
in Ireland (Caravaggiet al. 2015). Agricultural intensica-
tion is thought to be the primary cause of decline, result-
ing in the loss of herbaceous biodiversity required for
both food and shelter (Dingerkus and Montgomery 2002,
McGowanetal. 2019). e current population is estimated
at 223 000 hares (McGowanetal. 2019). While there is an
open hunting season, they are rarely taken as a game species
in the Republic of Ireland. However, hare coursing, whilst
banned in most countries, is a regulated and widespread
practice (Reidetal. 2007, 2010b, Kelly 2020). Despite their
cultural signicance, little research has been conducted on
the endoparasites of lagomorphs in Ireland. is is with the
exception of Butler (1994), who recorded the arthropod and
helminth parasites of rabbits Oryctolagus cuniculus.
Endoparasite infestations in lagomorphs reduce host sur-
vival by impacting on body condition and increasing pre-
dation (Murrayetal. 1997, Lello et al. 2005). Mountain
hares are known to host heavy helminth infestations and are
particularly susceptible to high burdens of the two gastro-
intestinal species Graphidium strigosum and Trichostrongylus
retortaeformis (Neweyetal. 2005). High levels of infestation
can negatively impact on female fecundity and are suspected
to be a contributor to the unstable population dynam-
ics observed in mountain hares (Newey et al. 2005). We
hypothesise that endoparasite communities in the Irish sub-
species will be similar to those recorded in other mountain
hare populations and the European rabbit. Here we describe
the endoparasite community and associated prevalence of
three helminth taxa from Irish hare carcasses opportunisti-
cally sourced from wildlife-strike incidents from the Repub-
lic of Ireland.
Methods
Carcass collection
A total of 22 Irish hare carcasses were examined, the major-
ity of which (n = 19) were obtained from Dublin Airport
(DUB, 53°42′64″N, 6°24′99″W), following fatal collisions
with aircraft (2010–2015). e grasslands at DUB are main-
tained using a ‘long grass’ management policy consisting of
a blend of tall fescue Festuca arundinacea and Italian ryegrass
Festuca perennis. Carcasses were collected by DUB person-
nel from runways and the conditions surrounding the strike
Wildlife Biology 2020: wlb.00717
doi: 10.2981/wlb.00717
© 2020 e Authors. is is an Open Access article
Subject Editor: Christian Sonne. Editor-in-Chief: Ilse Storch. Accepted 7 July 2020
is work is licensed under the terms of a Creative Commons
Attribution 4.0 International License (CC-BY) <http://
creativecommons.org/licenses/by/4.0/>. e license permits
use, distribution and reproduction in any medium, provided the
original work is properly cited.
2
incident recorded. Carcasses were recorded to have been col-
lected in the spring (n = 1), summer (n = 1), autumn (n = 2)
and winter (n = 9). Six carcasses from the aireld had no
date associated with them. Post collection, all carcasses were
immediately frozen. e carcasses were then made available
from the Dublin Airport Authority, in line with their policy
of making scientic use of wildlife-strike data (Kellyetal.
2017). A further three specimens were opportunistically col-
lected from road side accidents in the counties of Cork (n = 2)
(52°08′12″N, 8°86′32″W/52°06′70″N, 8°83′16″W) and
Tipperary (n = 1) (52°36′27″N, 7°58′80″W) in the winter
of 2014–2015.
Carcass processing
ere was an apparent preponderance of males (14 males,
1 female, 7 unknown) and adults (20 adults, 2 juveniles).
Due to the nature of the specimens’ deaths, some carcasses
were incomplete, resulting in a total of 13 whole hares and a
total of 15 complete digestive tracts (Table 1). All carcasses
were thawed for 24 h at room temperature prior to process-
ing. Where possible, specimens were identied to sex by
visual inspection and aged based on the presence or absence
of epiphyseal distal cartilage (Fernándezetal. 2010).
e digestive tract was sectioned into the 1) stomach, 2)
large intestine and 3) small intestine. e 4) heart, 5) lungs,
6) liver and 7) kidney were also examined and sectioned.
Digestive tract sections were separately opened and exam-
ined for macroparasites which were removed and counted
(Kornaś et al. 2014). Each section and digestive contents
were washed through successive sieves (250, 150 and 90 μm)
(Kornaśetal. 2014). Sieve contents were washed with 70%
ethanol into sample containers and parasites were counted
and identied under binocular microscope (Chroustetal.
2012). Cestodes were isolated from the small intestine,
without the presence of an intact scolex and were therefore
cleared and identied using other morphological features
against reference material. To count the number of cestodes
present in a host, the immature, smaller strobila at the ante-
rior end of the cestode were located and their presence con-
sidered to be a single cestode.
Statistical analysis
e full set of host specimens (n = 22) were used to deter-
mine the overall prevalence (%) of each parasite taxon. Only
intact specimens (n = 13) were used to determine parasite
burden and organ burden. Intact specimens (n = 13) were
used to examine the eect of parasite burden for each taxon
on host weight (g) and data were tested for normality using
the Shapiro–Wilk test. Kendall correlations were tted for
non-parametric data. All statistical analysis was carried out
in programme R ver. 3.6.1 (<www.r-project.org>). We
obtained Fisher’s index of aggregation (F = σ2/μ), where
F > 1 indicates an aggregated pattern, followed by a χ2-test.
To determine if parasite burdens were aggregated in the host
population, the ‘epiphy’ package (Gigot 2018) was used. We
did not investigate the eects of sex, age, season or location
on parasite burden due to the small sample size.
Results
In total, three endoparasite taxa were recorded in the Irish
hare with 50% being host to at least one taxon (Table 2).
Overall, 18% (n = 4) of hares were host to two parasite
taxa. Across all specimens (n = 22), Trichostrongylus retor-
taeformis was the most prevalent helminth (43%, n = 9) fol-
lowed by Graphidium strigosum (20%, n = 3). A tapeworm
belonging to the Mosgovoyia genus was also recorded (14%,
Table 1. Hare Lepus timidus hibernicus specimens opportunistically sourced from strike events with aircraft (n = 19) and vehicle (n = 3) colli-
sions in the Republic of Ireland. Due to the nature of the specimen’s deaths, not all carcasses were intact for analysis. Only the weights of
intact specimens are presented. Unk = Unknown.
ID Condition Age Sex Weight (g) Season Year Location
1* Intact Adult Unk 1680 Winter 2013 DUB
2* Intact Adult Male 1720 Winter 2013 DUB
3* Intact Adult Male 2020 Winter 2014 Clonmel, Co. Tipperary
4* Intact Adult Unk 2480 Winter 2014 Nad, Co. Cork
5* Intact Adult Male 2340 Winter 2014 Lyre, Co. Cork
6* Intact Adult Male 2140 Autumn 2014 DUB
7* Intact Adult Unk 2060 Winter 2014 DUB
8* Intact Adult Unkn 1995 Autumn 2014 DUB
9* Intact Adult Ukn 1980 Winter 2014 DUB
10* Intact Adult Male 2190 Winter 2015 DUB
11* Intact Adult Ukn 1825 Unk Unk DUB
12* Intact Adult Female 2965 Unk Unk DUB
13* Intact Juvenile Male 1320 Unk Unk DUB
14 Fragmented Adult Ukn NA Summer 2010 DUB
15 Fragmented Adult Ukn NA Spring 2014 DUB
16 Fragmented Adult Ukn NA Winter 2014 DUB
17 Fragmented Adult Ukn NA Winter 2014 DUB
18 Fragmented Adult Ukn NA Winter 2015 DUB
19 Fragmented Adult Ukn NA Winter 2015 DUB
20* Fragmented Adult Male NA Unk Unk DUB
21 Fragmented Juvenile Male NA Unk Unk DUB
22* Fragmented Adult Ukn NA Unk Unk DUB
* Indicates entire digestive tract.
3
n = 3). Trichostrongylus retortaeformis was the most numer-
ous helminth amounting to 99% of individual endoparasites
recorded.
Only hares sourced from DUB (n = 19) were positive
for helminths, with a mean burden of 292.7 (SE ± 163.64)
for infested intact specimens (n = 13). Although several
organs were examined, all parasites were conned to either
the stomach (G. strigosum) or the small intestine (T. retor-
taeformis, Mosgovoyia sp.). e small intestine had a higher
mean parasite burden of 262.3 (SE ± 163.9) than the stom-
ach (1.9 SE ± 1.3) in intact specimens (n = 13). e mean
weight of hosts examined was 2055 g (range 1320–2480 g),
with little dierence in the mean observed between seasons
(autumn = 2068 g, winter = 2059 g). ere was a weak cor-
relation between host parasite burden and body weight. is
correlation was not signicant for either T. retortaeformis
(r = −0.09, n = 13), G. strigosum (r = −0.09, n = 13) or the
Mosgovoyia tapeworm species (r = −0.17, n = 13). Parasite
burden was highly aggregated for all three parasites: T. retor-
taeformis (F = 769.4; χ2(12, 13) = 9232, p < 0.001); G. strigosum
(F = 10.4; χ2(12, 13) = 124.97, p < 0.01); and the Mosgovoyia
tapeworm species (F = 4.5; χ2(12, 13) = 54.71, p < 0.001).
Discussion
Here we identify three helminth endoparasite taxa hosted by
the endemic Irish hare. is is somewhat lower than studies
in continental Europe, where members of the genus Lepus
have been recorded to host between ve and 10 endopar-
asite taxa (Soveri and Valtonern 1983, Bordesetal. 2007,
Chroust et al. 2012, Lukešová et al. 2012, Diakouet al.
2014, Kornaśetal. 2014). It is possible that the Irish hares
geographic and genetic isolation from other mountain hare
populations (Hamilletal. 2006) may be a contributing fac-
tor to this low helminth diversity, as may the small sample
size from a predominantly single location (DUB). We do
not believe in this instance that season played a major role in
parasite diversity but it is known to impact on parasite bur-
den and aggregation (Neweyetal. 2005). Six helminth spe-
cies have been identied in rabbits in Ireland (Butler 1994),
three of which were present in hares included in this study,
conrming low host specicity.
Overall, 50% (n = 11) of hare specimens examined were
host to at least one parasite taxon, the most prevalent of
which was Trichostrongylus retortaeformis (43%, n = 9).
Higher prevalence rates of 99% (n = 589) have been found
in mountain hares in Scotland (Newey et al. 2005) and
76% (n = 109) in Finland (Soveri and Valtonern 1983). e
Mosgovoyia sp. is likely to be Mosgovoyia pectinata which
has been identied previously in rabbits in Ireland (But-
ler 1994) and mountain hares in Scotland (Hulbert and
Boag 2001). However, due to the absence of the scolex,
it was not possible to identify this cestode with certainty.
We found a Mosgovoyia species to be infecting 14% of Irish
hares, similar to levels recorded in Spain (17% (n = 487);
Segoviaet al. 2014). Contrastingly, we found Graphidium
strigosum prevalence (20%) to be higher than in other parts
of Europe, where prevalence has been recorded between 3%
(n = 225) and 4% (n = 137) (Chroustetal. 2012). However,
dierences in prevalence rates recorded between these stud-
ies and that of the Irish hare may be as a result of the small
sample size used (n = 22). All three parasite taxa recorded
in the Irish hare were aggregated (σ2 ≥ μ), which can inu-
ence individual tness, parasite transmission and popula-
tion regulation (Poulin 2013). For example, aggregation in
hares is highest during the winter months due to reduced
transmission rates and is thought to negatively impact on
body condition (Neweyetal. 2005).
We found that T. retortaeformis burden was not correlated
with host weight. Whilst we found no correlation to G. stri-
gosum burden and host weight, Allanetal. (1999) found a
positive correlation between increasing host weight and G.
strigosum burden, as a consequence of this parasite gener-
ally being associated with older individuals (Dudzinski and
Mykytowycz 1963). Interestingly, in this study a juvenile
yielded the highest G. strigosum burden.
Habitat type and quality have been shown to impact
on gastrointestinal helminth prevalence in mammals (Hul-
bert and Boag 2001, Froeschke and Matthee 2014, Santic-
chiaetal. 2015). erefore, it is not certain if the prevalence
rates recorded in this study are reective of the overall Irish
hare population or a reection of the habitat type (i.e. aireld
semi-natural grassland). e three parasite taxa recorded in
hares in this study are transmitted through the consump-
tion of vegetation contaminated with either free-living larvae
(T. retortaeformis and G. strigosum) or orbatid mites (Mosgo-
voyia sp.). Lagomorphs can share and potentially transmit
parasite species with commercially important ruminants
(Audebertet al. 2002), with evidence that they may trans-
mit anthelminthic resistant parasite strains between livestock
grazing areas (Stottetal. 2009). Data on the helminth fauna
of the Irish hare is, therefore, important from an agricultural
and habitat management perspective.
Table 2. Prevalence (%), mean intensity (μ ± SE) and range of infected hares Lepus timidus hibernicus for each endoparasite taxon identified
from 1) all hosts (n = 22) where not every target organ was available and 2) from intact specimens (n = 13) with all target organs available.
Parasite taxa Target organ and number
available Prevalence (%) Mean intensity (± SE) Range (n–n)
All specimens (n = 22 in total)
T. retortaeformis Small intestine (n = 21) 43 (n = 9) 868.7 (± 301.2) 112–2560
G. strigosum Stomach (n = 15) 20 (n = 3) 12.3 (± 0.8) 11–14
Mosgovoyia sp. Small intestine (n = 21) 14 (n = 3) 4.7 (± 1.2) 3–7
Intact specimens (n = 13)
T. retortaeformis Small intestine (n = 13) 38 (n = 5) 850 (± 428) 112–2000
G. strigosum Stomach (n = 13) 23 (n = 3) 12.5 (± 1.5) 11–14
Mosgovoyia sp. Small intestine (n = 13) 23 (n = 3) 5.0 (± 2.0) 3–7
4
Coursing is a standard practice in the Republic of Ireland
and is aliated with the administration of anthelmintic
treatments (e.g. Ivermectin) to wild populations of hares.
It is notable that in this study hares, albeit in small num-
bers, sourced in parts of the country distant from the airport
had no helminths. Two of these hares were not tagged and
so unlikely to have received anthelmintic treatments. An
ear tag conrmed that the remaining hare from Tipperary
had been coursed and therefore treated, but in a previous
year. Comparing the endoparasite community composi-
tion and parasite burden of Irish hares in the Republic to
those in Northern Ireland where coursing is not a regulated
practice, would give valuable insights into any population
level eects as a result of anthelminthic treatments. As the
endoparasite community of the Irish hare was unrecorded
until now, this study can help inform ongoing manage-
ment practices as to the appropriateness of these current
anthelminthic treatments being administered. We suggest
that the regular treatment of hares countrywide, over a pro-
longed period, has the potential to impact on parasite–host
dynamics.
Conclusion
Gaining an understanding of a species parasitofauna com-
position is important from both a resource management
and conservation perspective. In the case of the endemic
subspecies of Irish hare, we identied parasite species
known to impact on population dynamics (e.g. T. retor-
taeformis and G. strigosum). Further research is needed to
quantify the prevalence and range of the parasite commu-
nity of Irish hares across the island of Ireland. Such data is
crucial to investigate and understand the impact of current
treatment and management practices on hare population
dynamics in order to ensure continued conservation of this
iconic Irish mammal.
Acknowledgements – We would like to thank the Dublin Airport
Authority for providing carcasses for this study and to P. Whelan
and A. Haigh (UCC) for the opportunistic collection of roadside
specimens. e Irish Coursing Club kindly provided information
about the administration of anti-parasitic drugs.
Conict of interest – is work was conducted as part of a research
project in 2015. As of 2018 the lead author works with the Dublin
Airport Authority as a project partner to conduct PhD research.
Ethics – is article does not contain any studies with human
participants or live animals. All specimens were opportunistically
sourced from wildlife collisions.
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