International Journal for Parasitology: Parasites and Wildlife 17 (2022) 205–210

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International Journal for Parasitology: Parasites and Wildlife

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High Toxocara cati prevalence in wild, free-ranging Eurasian lynx (Lynx

lynx) in Finland, 1999–2015
Miisa Virta a, b, *, Otso Huitu c, Juha Heikkinen a, Katja Holmala a, 1, Pikka Jokelainen d, e, 1
a
Natural Resources Institute Finland, Latokartanonkaari 9, 00790, Helsinki, Finland
b
Faculty of Biological and Environmental Sciences, University of Helsinki, Viikinkaari 1, 00014, Helsinki, Finland
c
Natural Resources Institute Finland, Korkeakoulunkatu 7, 33720, Tampere, Finland
d
Infectious Disease Preparedness, Statens Serum Institut, Artillerivej 5, DK-2300, Copenhagen, Denmark
e
Faculty of Veterinary Medicine, University of Helsinki, Agnes Sjöberginkatu 2, 00014, Helsinki, Finland

A R T I C L E I N F O A B S T R A C T

Keywords: In Finland, free-ranging Eurasian lynx (Lynx lynx) population has grown from 30 to 40 individuals to 2800 in­
Eurasian lynx dividuals since the species became partly protected in 1962. Changes in host population size are known to have
Population growth an impact on host-parasite dynamics, and the Eurasian lynx population in Finland provides a unique opportunity
Host-parasite dynamics
for studying the potential effects of dramatic population increase and expansion of a solitary apex predator on
Toxocara cati
their parasite prevalence and abundance. Toxocara cati is a zoonotic gastrointestinal parasite infecting domestic
cats and wild felids worldwide. We studied T. cati infection prevalence and worm burden in 2756 Eurasian lynx
individuals from Finland, covering the years 1999–2015. Toxocara cati worms that had been collected from
intestinal contents were identified based on morphology. We performed regression analyses to investigate
possible associations of age, sex, and host population density with T. cati infection. We found T. cati from 2324
(84.3%, 95% confidence interval 82.9–86.0) of the examined lynx. Each year, the infection prevalence was
higher than 75% and not density dependent. The parasites were strongly aggregated, with older individuals
harboring fewer T. cati than younger ones did. Old females aged 9–15 years had higher T. cati abundance than
males of the same age group. Our results indicate that T. cati was a common and abundant parasite of Eurasian
lynx throughout the study period, regardless of the changing population size and density.

1. Introduction Both felids and humans can become infected with T. cati by ingesting
embryonated eggs of the parasite or by eating tissues of paratenic hosts
The zoonotic gastrointestinal nematode Toxocara cati is a common (Sprent, 1956; Overgaauw et al., 1997; Fisher, 2003; Coati et al., 2004;
parasite infecting domestic cats as well as wild felids worldwide (Sprent, Davidson et al., 2012; Strube et al., 2013). Moreover, kittens of domestic
1956; Bagrade et al., 2003; Valdmann et al., 2004; Sommerfelt et al., cats can become infected via milk (Swerczek et al., 1971).
2006; Zibaei et al., 2007; Okulewicz et al., 2012; Gallas and Silveira, Parasite prevalence and abundance tend to follow host population
2013; Otranto and Deplazes, 2019; Hou et al., 2020; Figueiredo et al., size and density (May and Anderson, 1979; Dobson and Hudson, 1992;
2021; Ursache et al., 2021). In Finland, the prevalence of T. cati in do­ Arneberg et al., 1998). It is assumed that host-parasite dynamics follow
mestic cats was estimated to be 5.4%, based on detection of eggs of the the Lotka-Volterra predator-prey model: changes in the population size
parasite in feces (Näreaho et al., 2012). Toxocara cati is a common of a prey or a host are followed by changes in the population size of a
parasite also of free-ranging Eurasian lynx (Lynx lynx) in the country predator or a parasite (Anderson and May 1978; Dobson and Hudson,
(Deksne et al., 2013). Data on T. cati prevalence in both domestic cats 1992). However, there are only few studies on how population increase
and wild felids are needed to understand the circulation of the parasite and expansion of large carnivores has affected their parasites. For
and the zoonotic and cross-species infection risks. example, in Germany, parasite prevalence and diversity in wolves

* Corresponding author. Natural Resources Institute Finland, Latokartanonkaari 9, 00790, Helsinki, Finland.
E-mail addresses: [Link]@[Link] (M. Virta), [Link]@[Link] (O. Huitu), [Link]@[Link] (J. Heikkinen), [Link]@[Link] (K. Holmala),
PIJO@[Link] (P. Jokelainen).
1
These authors contributed equally.

[Link]
Received 17 November 2021; Received in revised form 6 February 2022; Accepted 7 February 2022
Available online 9 February 2022
2213-2244/© 2022 The Authors. Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an open access article under the CC BY license
([Link]
M. Virta et al. International Journal for Parasitology: Parasites and Wildlife 17 (2022) 205–210

increased with advancing recolonization process (Leshniak et al., 2017). 2. Materials and methods
Age and sex of the host are also known to have an impact on parasite
abundance and intensity (Kołodziej-Sobocińska, 2019). Juveniles still 2.1. Study setting and design
developing acquired immunity can be more heavily infected and have
higher prevalence than adults (Hudson and Dobson, 1995; Gates and The study was a retrospective observational study. The data included
Nolan, 2009; Reinemeyer and Nielsen, 2017). In older individuals, parasite worms collected from intestines of 2756 Eurasian lynx that had
declining immune function may explain higher parasite burden (Froy been legally hunted or had died in e.g. car collisions in Finland in
et al., 2019). Sex-biased parasitism is common in many mammal species 1999–2015. No animals were killed for the purpose of this study. All
(Moore and Wilson, 2002; Krasnov et al., 2005). The differences in procedures were performed in compliance with relevant laws and
immunity, prey selection, feeding habits, home range size, and hor­ guidelines.
mones can to some extent explain differences in parasitism between The Eurasian lynx is protected in Finland. Hunting is permitted for
sexes (Poulin, 1996; Hillegass et al., 2008; Friesen et al., 2015; Kojola damage control and for population management purposes. Yearly quota
et al., 2017; Albery et al., 2020). In females, estrogen stimulates im­ is set by Ministry of Forestry and Agriculture, and permits are annually
munity, whereas in males the major androgen testosterone is an issued by Finnish Game Agency for the 15 game managements districts
immunosuppressive hormone and therefore supports male-biased (GMD), based on the estimated lynx population size in each GMD.
parasitism (Schuurs and Verheul, 1990; Poulin, 1996). Population size estimation is based on observed number of litters
Parasites often exhibit an aggregated distribution within their host (Natural Resources Institute Finland, 2016). The hunting period is from
population – a few hosts harbor many parasites, whereas most hosts the beginning of October to the end of February in reindeer herding
have none or only a few parasites (Crofton, 1971; Shaw and Dobson, area, and from the beginning of December to the end of February in
1995; Morand and Krasnov, 2008). Factors such as age and season can other areas. Data from 14 GMDs were included in the present study;
influence the degree of parasite aggregation (Hudson et al., 1992; Boag GMD covering Lapland in northern Finland was excluded due to limited
et al., 2001; Saeed and Kapel, 2006; Sherrard-Smith et al., 2015). The sample size and non-comparable estimates of population size.
effect of age may be related to immunity, and the seasonal changes to Frozen carcasses of Eurasian lynx were sent by hunters and officials
weather conditions, which can affect infective stages of the parasites or to Taivalkoski research station of Natural Resources Institute Finland.
intermediate hosts (Hudson et al., 1992; Boag et al., 2001; Fromont The carcasses were dissected and the whole gastrointestinal tract was
et al., 2001; Newey et al., 2005). searched for parasitic worms. The intestinal contents were rinsed with
Previous studies have shown that Eurasian lynx in Finland are hosts water on a fine mesh sieve, and all visible gastrointestinal parasitic
to protozoa including Toxoplasma gondii and Isospora sp., nematodes worms were collected. Nematodes were separated from cestodes based
including T. cati and Trichinella spp., and cestodes including Taenia spp. on morphology, and counted. The worms were stored in 70% ethanol at
and Mesocestoides sp. (Oksanen et al., 1998; Airas et al., 2010; Deksne +8 ◦ C temperature. The age of each individual lynx was determined
et al., 2013; Jokelainen et al., 2013; Lavikainen et al., 2013; Haukisalmi based on analysis of cementum annuli of their teeth by the Matson
et al., 2016; Kojola et al., 2017). In particular, T. cati was found to be a Laboratory, Montana, USA (Matson, 1981).
highly prevalent parasite, found from intestines of 92.9% of investigated We identified T. cati parasites based on the key morphological fea­
Eurasian lynx (Deksne et al., 2013), which is in line with findings from tures with focus on their anterior end, in particular the shape and po­
other countries (Bagrade et al., 2003; Valdmann et al., 2004; Kołod­ sition of cephalic alae (Sprent, 1956), and recorded their absence or
ziej-Sobocińska et al., 2018). presence and numbers. Cestode absence/presence was included in the
The Eurasian lynx population size in Finland decreased in the early analyses as a dichotomous variable to investigate co-infections.
20th century due to hunting (Pulliainen and Rautiainen, 1999). The
species became partly protected in 1962, at a time when the estimated 2.2. Statistical analyses
population size was only 30–40 individuals, predominately living in
south-eastern Finland (Pulliainen and Rautiainen, 1999). The protection The presence of T. cati was treated as a binary variable (absence/
together with a change in prey species to increasingly available presence). We report prevalence, abundance and intensity. Apparent
white-tailed deer (Odocoileus virginianus) and European roe deer (Cap­ T. cati infection prevalence was defined by dividing the number of
reolus capreolus) enabled the Eurasian lynx population size to increase, Eurasian lynx that had T. cati infection by the number of examined
reaching approximately 855 individuals in 1995 (Pulliainen, 1981) and Eurasian lynx. Abundance denotes the number of T. cati parasites in any
2800 individuals in 2013 (Natural Resources Institute Finland, 2014). In given lynx individual, while intensity denotes the number of T. cati
eastern Finland, hares (Leporidae) and grouse (Tetraonidae) are the parasites in an infected lynx (Bush et al., 1997).
main prey of Eurasian lynx, whereas in southern and south-western Logistic regression was used to analyze the relationship between
Finland the typical diet includes equal proportions of hares and small T. cati presence and the age of the lynx (continuous variable), the sex of
cervids (Cervidae) (Pulliainen et al., 1995). the lynx, the year when the lynx was hunted, the presence of cestodes,
The history of Eurasian lynx population in Finland provides an op­ and GMD-level lynx population density index. The lynx population
portunity to study the potential effects of dramatic population increase density index was calculated by dividing the annual Eurasian lynx
and expansion of a solitary apex predator on their parasite prevalence population size estimate of each GMD by the area, in km2, of the GMD.
and abundance. The aim of this study was to describe T. cati prevalence Data on T. cati abundance were non-normally distributed and zero
and abundance in Eurasian lynx in Finland over a 16-year study period, inflated. Generalized linear mixed models with negative binomial
while the lynx population size increased. We hypothesized that the in­ regression were used to analyze the relationship between T. cati abun­
crease in host population size and density would be positively associated dance and age, sex, presence of cestodes, and lynx population density
with T. cati prevalence and abundance. We estimated the prevalence by index. The year the lynx was hunted or had died and the GMD were
year and investigated whether age and sex of the lynx were associated included as random effects. Because T. cati abundance and age had a
with having the infection. We hypothesized that young Eurasian lynx significant relationship with a second degree polynomial involving age
would have higher T. cati prevalence than older ones, and that males squared, both age and age squared were fitted as explanatory variables
would have higher prevalence than females. into the analysis of variation of worm abundance.
⎛
⎜
The aggregation parameter k was calculated with the model ⎜
⎝k =

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⎞
There was a significant negative association between age of the lynx
2
μ2 − σN ⎟
⎟, and T. cati abundance (Coef. = − 0.191, p < 0.001, SE = 0.028, df = 1, F
(σ 2 − μ)⎠
which was originally described by Fisher (1941) and Bliss and
= 45.80). The worm abundance was significantly lower amongst older
lynx. Lynx density did not have a significant effect on worm abundance
Fisher (1953), and further modified by Elliott (1971) by including (p = 0.434). The variance of the random effect for the years was different
sample size (N), which gives better estimation for the k (Buhat et al., from zero, indicating the years were different in regards to T. cati
2020). The variance in the model is σ and the mean is μ. If k approaches abundance.
zero and is less than one, it is an indicator of a highly aggregated parasite Age squared and T. cati abundance were significantly positively
population (Shaw and Dobson, 1995; Buhat et al., 2020). associated (Coef. = 0.008, p = 0.011, SE = 0.003, df = 1, F = 17.71).
The statistical analyses were performed with SPSS 27 (IBM Corpo­ There was an interaction with T. cati abundance, age squared, and sex (p
ration, New York, USA). = 0.009, SE = 0.003, df = 1, F = 11.13). Females aged 9–15 years had a
significant positive relationship with T. cati abundance (Coef. = 1.298, p
3. Results < 0.001, SE = 0.374, df = 5, F = 3.53), while the abundance was not
related to age in males. Among the total of 67 lynx aged 9–15 years, the
3.1. Toxocara cati prevalence mean abundance was 26.0 (range 0–162) in the 40 females and 7.5
(range 0–42) in the 27 males (Fig. 3).
Parasitic worms were found in 2565 (93.1%, 95% confidence inter­ There was a positive relationship between T. cati abundance and
val (CI) 92.1–94.0) of the 2756 examined Eurasian lynx. Toxocara cati presence of cestodes, indicating a higher probability of co-infection
infection (Fig. 1) was detected in 2324 of the lynx, yielding an apparent when T. cati abundance was higher (Coef. = 0.377, p < 0.001, SE =
infection prevalence of 84.3% (95% CI 82.9–86.0) (Table 1). Cestode 0.067, F = 31.93).
infection was detected in 2023 (74.0%, 95% CI 72.4–75.7) of the lynx.
Toxocara cati prevalence was high throughout the years, varying 4. Discussion
from 77.2% (95% CI 70.4–84.0) in 2009 to 92.3% (95% CI 84.8–99.8) in
2006 (Fig. 2). The prevalence was over 80% in most of the years and did This longitudinal study using exceptionally large data gives exten­
not vary statistically significantly between the years (p = 0.905), sive new insight to the host-parasite dynamics of wild, free-ranging
although the Eurasian lynx population size increased (Fig. 2). Eurasian lynx and the zoonotic nematode T. cati. Unexpectedly, T. cati
The proportion of Eurasian lynx infected with T. cati was high in all prevalence was not dependent on lynx population size, but instead
age groups (Table 1). There was a significant negative association be­ remained high across the years – while the lynx population size tripled
tween presence of T. cati and age (Coef. = − 0.070, p = 0.002, standard (Fig. 2). Toxocara cati abundance was not dependent on lynx population
error (SE) = 0.023, df = 1, F = 93.73). The prevalence of T. cati did not density either. These observations represent an important addition to
differ statistically significantly between sexes (p = 0.778). There was a our understanding on parasites in relation to host population size, as
significant positive relationship between the presence of T. cati and the they contrast what is expected based on established literature (May and
presence of cestodes (Coef. = 1.172, p < 0.001, SE = 0.121, df = 1, F = Anderson, 1979; Dobson and Hudson, 1992; Arneberg et al., 1998).
93.73). Lynx density index did not appear to be a significant factor (p = While the observations are supported by the collected data, they may be
0.812). No interactions were detected between the investigated factors. partly explained by the lynx density not reaching a relevant threshold or
by the territorial behavior of the lynx. With the exception of females
with cubs, adult Eurasian lynx live a solitary life, have large home
3.2. Toxocara cati abundance and intensity
ranges, and display intrasexual territoriality whereby especially adult
males have a tendency to avoid conspecifics (Schmidt et al., 1997;
The mean T. cati abundance was 18.0 (standard deviation = 25.5),
Linnell et al., 2001; Herfindal et al., 2005; Breitenmoser-Würsten et al.,
and the mean T. cati intensity was 21.2 (standard deviation = 26.0)
2007).
(Table 1). The parameter k for parasite aggregation was 0.513 indicating
Toxocara cati prevalence remained high throughout the study period
highly aggregated parasite distribution.
and varied relatively little by year (Fig. 2). This might be explained
either by T. cati being co-introduced with the lynx to an empty niche, or
by a high infection pressure. Co-introduction of parasites and their hosts
is a common phenomenon when hosts are invasive, introduced, or
immigrating to new or empty niches (Williamson and Griffiths, 1996;
Laurimaa et al., 2016; Lesniak et al., 2017). On the other hand, T. cati life
cycle is well-established and maintained in Finland with contributions
by domestic cats (Kauhala et al., 2015; Näreaho et al., 2012). While little
is known on the level of local environmental contamination with T. cati
eggs as well as on the prevalence of the infection in relevant paratenic
hosts, the parasite is endemic and can infect the dispersing lynx.
Toxocara cati infection was highly prevalent in Eurasian lynx of all
age groups and both sexes (Table 1). Our hypotheses of age-dependent
and male-biased parasitism were not supported. Similar results have
been reported earlier from Finland: in a cross-sectional study the pro­
portion of individuals harboring T. cati worms was found to be almost
the same in sub-adult and adult lynx, and in lynx of both sexes (Deksne
et al., 2013).
The abundance of T. cati was significantly lower in older lynx and,
interestingly, older females aged 9–15 years harbored a significantly
Fig. 1. The head, the cephalic alae and the body of the Toxocara cati found higher number of T. cati nematodes than males of the same age group
from female Eurasian lynx (Lynx lynx) from Finland. The measurement scale (Fig. 3). The mean intensity of T. cati was lower in lynx in the oldest age
has red marks at 1 mm intervals. (For interpretation of the references to colour group than in younger lynx (Table 1). This is in contrast to the findings
in this figure legend, the reader is referred to the Web version of this article.) from Estonia, where no significant difference in T. cati intensity was

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Table 1
Number of examined Eurasian lynx (Lynx lynx), number of Toxocara cati positive lynx, T. cati prevalence, abundance (mean, standard deviation), intensity (mean,
standard deviation, median, range), and parameter k as an aggregation indicator.
Number of Number of Prevalence Abundance, Abundance, Intensity, Intensity, Intensity, Intensity, Parameter
lynx Toxocara cati (%) mean standard mean standard median range k
examined positive lynx deviation deviation

Age ~6 645 543 84.2 18.4 28.0 22.0 29.2 11.0 1–218 0.444
months
Age 1–2 1276 1096 85.9 21.0 26.9 24.3 26.9 15.5 1–213 0.628
years
Age 3 835 685 82.0 12.9 19.7 15.7 20.7 8.0 1–183 0.442
years
and
over

Female 1138 959 84.3 18.0 25.6 21.2 25.7 13.0 1–213 0.511
Male 1618 1365 84.4 17.9 25.4 21.2 26.2 12.0 1–218 0.517

Total 2756 2324 84.3 18.0 25.5 21.2 26.0 12.0 1–218 0.513

sample included a good number of older individuals, while one age

group that was not included in our study was young cubs.
The parasites were strongly aggregated, which in line with previous
studies that have reported parasite aggregation of intestinal worms in
mammalian hosts (Newey et al., 2005; Saeed and Kapel, 2006). The
differences between age groups and between sexes were relatively small.
We were unable to analyze the effect of seasonality on aggregation
because the sampling was largely linked to hunting seasons.
The detection of parasitic worms relied on their visibility, and
smaller parasites may have been missed. Moreover, the carcasses were
frozen, and the freezing and thawing may have affected the success of
detecting all parasitic worms. Our results may thus be an underestima­
tion of prevalence, abundance and intensity; however, as the procedures
were the same throughout the study period and for all the animals
investigated, the data are comparable across years and between indi­
vidual hosts.
Interestingly, Eurasian lynx with higher T. cati abundance were more
Fig. 2. The estimated Eurasian lynx (Lynx lynx) population size and Toxocara
likely to be co-infected with cestodes. Similar results have been found in
cati prevalence (%, 95% confidence interval) in Finland, by year. domestic cats in Finland: cats that shed cestode eggs in their feces had
higher odds of shedding Toxocara or Toxascaris eggs than cats that did
not shed cestode eggs in their feces (Näreaho et al., 2012). Several
cestode species have been described in the Eurasian lynx, including
Taenia spp. and Mesocestoides sp. (Deksne et al., 2013; Lavikainen et al.,
2013; Haukisalmi et al., 2016).
Toxocara cati is a zoonotic parasite that can cause toxocariasis in
humans (Despommier, 2003; Fisher, 2003; Holland, 2017). Compared
with T. canis, T. cati has been receiving less attention both as a parasite of
veterinary importance and as a zoonotic parasite (Fisher, 2003; ESCCAP,
2021; Maciag et al., 2022). It is worth emphasizing that routine sero­
logical methods cannot distinguish between infections caused by T. canis
and T. cati, and the public health importance of T. cati is not fully
elucidated (Fisher, 2003; Poulsen et al., 2015; Maciag et al., 2022).
In felids, most T. cati infections are subclinical. In domestic cats,
heavy T. cati infection can cause clinical signs including pot-bellied
appearance, diarrhea, vomiting and inappetence (ESCCAP, 2021; Urs­
ache et al., 2021). Toxocara spp. has been reported as the cause of death
of two juvenile Eurasian lynx in Switzerland (Schmidt-Posthaus et al.,
2002). It cannot be ruled out that the infections in Eurasian lynx could
Fig. 3. Number of Toxocara cati worms in Eurasian lynx (Lynx lynx) in Finland, have potential effect on mortality and could have introduced bias in this
by age and sex. Median, first and third quartiles, and minimum and maximum
study, but as most of the detected infections were light, they were un­
are shown.
likely to have predisposed the individuals to hunting or traffic accidents.
Our results indicate that Eurasian lynx contribute to the circulation
observed between young and adult lynx (Valdmann et al., 2004). For of T. cati in Finland, which has both potential public health and animal
interpreting this and other comparisons, it should be emphasized that health importance. This highlights that free-ranging wildlife species
our age group categories differ from other studies; we had sufficient data should not be forgotten in the One Health investigations and approaches
for biologically relevant age groups. Eurasian lynx in Finland typically targeting zoonotic pathogens such as T. cati.
start to reproduce at the age of three years (Holmala, unpublished). Our

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