License to Kill? Domestic Cats Affect a Wide Range of Native Fauna in a Highly Biodiverse Mediterranean Country

Abstract

Amongst domestic animals, the domestic cat, Felis catus, is widely considered to be one of the most serious threats to wildlife conservation. This is particularly evident for island ecosystems, as data for mainland countries are often lacking. In Italy, the European country that is richest in biodiversity, cats are very popular pets. In this work, we aimed at assessing the potential spectrum of wild vertebrates that may be killed by free-ranging domestic cats, and we considered our results within the context of their conservation status and IUCN threat category. We collected data on the impact of cats both through a citizen science approach (wildlife predations by 145 cats belonging to 125 owners) and by following 21 of these 145 cats for 1 year and recording all of the prey they brought home. Domestic cats may kill at least 207 species (2042 predation events) in Italy; among those, 34 are listed as “Threatened” or “Near Threatened” by the IUCN and Italian Red Lists. Birds and mammals such as passerines and rodents were reported to be the groups most commonly killed by free-ranging cats. When considering this diet in functional trait space, we observed that the class occupying the largest functional space was that of birds, followed by mammals, reptiles, and amphibians. Thus, the largest impact was on the functional structure of mammal and bird communities. The use of a collar bell did not affect the predation rate of cats, and the number of prey items brought home decreased with increasing distance from the countryside. We provided strong evidence that free-ranging domestic cats may seriously affect the conservation of threatened and non-threatened wildlife species, which are already suffering from population declines due to other causes, e.g., habitat loss. The mitigation of the impacts of domestic cats on wildlife requires dissemination projects promoting responsible cat ownership, as well as a restriction of free-ranging behavior, particularly at nighttime.

Full text

ORIGINAL RESEARCH
published: 13 December 2019
doi: 10.3389/fevo.2019.00477
Frontiers in Ecology and Evolution | www.frontiersin.org 1December 2019 | Volume 7 | Article 477
Edited by:
Franco Andreone,
Museo Regionale di Scienze
Naturali, Italy
Reviewed by:
Giovanni Amori,
Italian National Research Council
(CNR), Italy
Giuseppe Bogliani,
University of Pavia, Italy
*Correspondence:
Emiliano Mori
moriemiliano@tiscali.it
†These authors have contributed
equally to this work
Specialty section:
This article was submitted to
Conservation,
a section of the journal
Frontiers in Ecology and Evolution
Received: 02 May 2019
Accepted: 25 November 2019
Published: 13 December 2019
Citation:
Mori E, Menchetti M, Camporesi A,
Cavigioli L, Tabarelli de Fatis K and
Girardello M (2019) License to Kill?
Domestic Cats Affect a Wide Range of
Native Fauna in a Highly Biodiverse
Mediterranean Country.
Front. Ecol. Evol. 7:477.
doi: 10.3389/fevo.2019.00477
License to Kill? Domestic Cats Affect
a Wide Range of Native Fauna in a
Highly Biodiverse Mediterranean
Country
Emiliano Mori 1
*†, Mattia Menchetti 2,3† , Alberto Camporesi 4, Luca Cavigioli 5,
Karol Tabarelli de Fatis 6and Marco Girardello 7
1Dipartimento di Scienze della Vita, Università degli Studi di Siena, Siena, Italy, 2Institut de Biologia Evolutiva, Consejo
Superior de Investigaciones Cientificas - Universitat Pompeu Fabra, Barcelona, Spain, 3Dipartimento di Biologia, Università di
Firenze, Sesto Fiorentino, Italy, 4Associazione per la Divulgazione Ambientale e Scientifica, Dovadola, Italy, 5Società di
Scienze Naturali del Verbano Cusio Ossola, Museo di Scienze Naturali, Collegio Mellerio Rosmini, Domodossola, Italy,
6MUSE – Museo delle Scienze, Corso del Lavoro e della Scienza, Trento, Italy, 7cE3c–Centre for Ecology, Evolution and
Environmental Changes/Azorean Biodiversity Group and Universidade dos Açores, Faculty of Agriculture and Environment,
Angra do Heroísmo, Portugal
Amongst domestic animals, the domestic cat, Felis catus, is widely considered to be
one of the most serious threats to wildlife conservation. This is particularly evident for
island ecosystems, as data for mainland countries are often lacking. In Italy, the European
country that is richest in biodiversity, cats are very popular pets. In this work, we aimed
at assessing the potential spectrum of wild vertebrates that may be killed by free-ranging
domestic cats, and we considered our results within the context of their conservation
status and IUCN threat category. We collected data on the impact of cats both through
a citizen science approach (wildlife predations by 145 cats belonging to 125 owners)
and by following 21 of these 145 cats for 1 year and recording all of the prey they
brought home. Domestic cats may kill at least 207 species (2042 predation events) in
Italy; among those, 34 are listed as “Threatened” or “Near Threatened” by the IUCN and
Italian Red Lists. Birds and mammals such as passerines and rodents were reported to
be the groups most commonly killed by free-ranging cats. When considering this diet in
functional trait space, we observed that the class occupying the largest functional space
was that of birds, followed by mammals, reptiles, and amphibians. Thus, the largest
impact was on the functional structure of mammal and bird communities. The use of
a collar bell did not affect the predation rate of cats, and the number of prey items
brought home decreased with increasing distance from the countryside. We provided
strong evidence that free-ranging domestic cats may seriously affect the conservation
of threatened and non-threatened wildlife species, which are already suffering from
population declines due to other causes, e.g., habitat loss. The mitigation of the impacts
of domestic cats on wildlife requires dissemination projects promoting responsible cat
ownership, as well as a restriction of free-ranging behavior, particularly at nighttime.
Keywords: Felis catus, alien species impacts, responsible pet ownership, predation rate, feral species

Mori et al. Impacts of Free-Ranging Cats in Italy
INTRODUCTION
Understanding the processes shaping ecological communities
under multiple disturbances is a crucial challenge in ecology
and conservation biology (e.g., Davis et al., 2000; Cilleros et al.,
2016; Mazel et al., 2017). Biological invasions represent a serious
threat to global biodiversity at all organization levels, from
genes to ecosystems (Wonham, 2006). By definition (Wonham,
2006), domestic species should also be considered “alien” when
they establish free-ranging populations in the wild outside
their native range (Carthey and Banks, 2012; Home et al.,
2017; Boano et al., 2019). The presence of domestic free-
ranging animals may disrupt ecosystems or contribute to local
extinction events (Malo et al., 2011). The impacts of feral
pets include environmental/habitat alterations (e.g., rabbits: Flux
and Fullagar, 1992; pigeons: Boano et al., 2019), predation
of native fauna (e.g., cats: Loss et al., 2013; dogs: Doherty
et al., 2017), hybridization with related wild species (e.g., ferrets:
Davison et al., 1999; cats: Randi et al., 2001; dogs: Bassi
et al., 2017), and disease transmission (e.g., ducks: Hinshaw
et al., 1978; cats: Loss and Marra, 2017). Among mammalian
invaders, domestic carnivores, e.g., dogs (Canis familiaris) and
cats (Felis catus), are reported to exert the most serious damage
(Van’t Woudt, 1990; Doherty et al., 2016; Home et al., 2017).
Furthermore, their management is challenging because of their
association with humans and their consequent appeal to the
public (Green and Gipson, 1994; Natoli, 1994; Thomas et al.,
2013). Negative impacts of free-ranging dogs are well-known
and commonly accepted to occur by the general public (Young
et al., 2011; Hughes and Macdonald, 2013), as dogs may also
attack humans (Scott and Causey, 1973; Home et al., 2017),
whereas negative impacts by domestic cats are often denied or
justified by the public as a form of “natural predatory instinct”
(Hall et al., 2016).
Across the globe, the domestic cat, Felis catus, is the
most popular pet. The Ecology Global Network estimates that
there are 600 million-1 billion domestic cats in the world,
including pets (i.e., largely dependent on human-provided food),
strays/homeless (i.e., poorly dependent on human-provided
food), and feral cats (totally independent from humans),
throughout all of the continents except for Antarctica (www.
ecology.com). The behavioral and physiological plasticity of
domestic cats allows them to survive even without food provided
by humans, both in urban areas and natural environments
(Gillies, 2001; Harper, 2005; Cove et al., 2018). Most studies on
the ecological impacts of domestic cats have been conducted in
island ecosystems (Liberg, 1984; Woods et al., 2003; Bonnaud
et al., 2011; Medina et al., 2011), where domestic cats are
responsible for the decline of many seabirds (Keitt et al.,
2002; Hughes et al., 2008; Bonnaud et al., 2009; Faulquier
et al., 2009) and for the local extinction of other terrestrial
vertebrates (Fitzgerald and Turner, 2000; Blackburn et al., 2004;
Medina and Garcìa, 2007; Medina et al., 2011; Kutt, 2012).
Free-ranging domestic cats may affect bird fecundity through
non-lethal indirect effects, i.e., by increasing stress (Bonnington
et al., 2013). An increase in prey species populations after cat
removal from islands suggests that domestic cats represent a
major source of predation in such ecosystems (Gillies, 2001;
Hughes et al., 2008; Siracusa, 2010). Birò et al. (2005) found
a low trophic niche overlap between feral cats and wild cats
Felis silvestris, suggesting the occurrence of niche partitioning
between the two. Conversely, domestic cats are opportunistic
predators, therefore showing a selective advantage over wild
cats, which are specialized to preying upon rodents (Birò et al.,
2005; Széles et al., 2018). Moreover, house-based domestic cats
are often free to move around outside and may increase the
predatory pressure exerted on wildlife (Pearre and Maass, 1998).
Domestic cats frequently kill wild animals without consuming
them and frequently bring prey home as a “gift” to their owners
(Meek, 1998; Woods et al., 2003). Unlike feral cats, house cats
are provided with medical care and shelter by pet owners, so
they are not subjected to fluctuations in prey abundances and
are therefore able to surpass the environmental carrying capacity
(Woods et al., 2003; Tschanz et al., 2011). Furthermore, domestic
cats may rapidly revert to the feral state, maintaining their
populations without human food supply (Birò et al., 2005; Széles
et al., 2018). The use of collars with a bell has been reported
to be a useful method for reducing wildlife killing by domestic
cats (Calver et al., 2007; Gordon et al., 2010). Given the impacts
detected in areas relatively poor in biodiversity (e.g., 1.4–3.7
billion birds and 6.9–20.7 billion mammals killed per year in
the continental USA: Loss et al., 2013), an even stronger effect
may be expected for biodiversity hotspot areas (cf. Home et al.,
2017) such as the Mediterranean basin (Myers et al., 2000).
Within this area, Italy hosts the highest animal species richness
(Oosterbroek, 1994; Maiorano et al., 2007) as well as a high
domestic cat density (nearly 10 million domestic cats: https://
pets.thenest.com; accessed on 7th April 2018), and yet evidence of
the effects of cats on wildlife is still poorly documented (Siracusa,
2010; Ancillotto et al., 2013).
Traditionally, ecologists have studied the relationships
between the severity of impacts of invasive species and the
taxonomic structure of animal communities (e.g., Sanders et al.,
2003; Hejda et al., 2009). Recent advances in the application of
frameworks based on species traits have provided an alternative
approach that allows researchers to quantify responses to
disturbances across taxa and ecosystems (Oliver et al., 2015).
Quantifying the impacts of invasive species on the functional
structure of communities is important for elucidating the
mechanism underpinning invasion processes, as well as for
improving researchers’ ability to predict the impacts of invasive
species on ecosystem functioning (Tilman et al., 1997).
In this work, we conducted a citizen science study to assess the
impact of domestic cat predation on the functional structure of
vertebrate communities in Italy by using a trait-based approach.
Specifically, the aims of this study were to (i) quantify the
predatory pressure of domestic cats on vertebrate prey in relation
to landscape features, and (ii) assess the effect of cat predation on
the functional structure of vertebrate communities. We suggested
that the highest number of species killed by free-roaming cats
would occur in countryside areas and in southern regions, where
the highest species richness is known to occur (Blasi et al., 2014;
Genovesi et al., 2014). Moreover, we also predicted that, given the
results of previous studies, cats with a bell on their collars (Calver
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Mori et al. Impacts of Free-Ranging Cats in Italy
FIGURE 1 | Locations of 21 cat owners who monitored the prey their cats returned over the course of 1 year (January–December 2016).
et al., 2007; Gordon et al., 2010) would kill fewer individuals and
species than those without bells.
MATERIALS AND METHODS
Citizen Science Survey
We carried out a citizen science survey to collect data
on wild species killed by domestic cats. The project was
advertised through mailing lists (“Italian vertebrates”:
vertebrati@liste.cilea.it), specific Facebook groups dealing
with wildlife in Italy (Table S1), flyers in universities (Pisa, Siena,
Florence, Rome, Milan, Turin, Pavia, and Catania), wildlife
agencies, catteries, and human meeting places. The survey was
also conducted using online platforms and social networks
(Facebook, Twitter) to gather information about domestic cat
predation on wildlife in Italy. In detail, participants were asked to
provide us with photographs of predation by their domestic cats,
with collection between 2014 and 2017. The project was launched
in spring 2014 and kept open until the end of 2017: only data
supported by photographs and attached coordinates were kept
for analyses. We did not ask for any further information from
the cat owners to avoid privacy issues. Environmental variables
were obtained by plotting coordinates on satellite maps. We also
followed up with targeted questions to contributors to increase
the reliability and adequacy of our survey (cf. Home et al., 2017).
Among the surveyed cat owners, we recruited a total of
21 volunteers (Figure 1) through Facebook groups, listed in
Table S1, to monitor predation events by single cats throughout 1
year (January-December 2016) by recording and photographing
all prey items brought home by the owned cat. These data were
also added to the citizen science project described above. The
owners of the 21 cats also gave us information on their cats,
including sex, use of collars with bells, and average period of
outdoor access (hours/day: cf. Frank et al., 2016).
Prey species were grouped according to the International
Union for the Conservation of Nature (IUCN) Red List (www.
iucnredlist.org; accessed on 11.02.2019) and the Italian Red List
(Rondinini et al., 2013).
Data Analysis on the Citizen Science
Survey
This analysis was carried out on the killings by the 21
cats followed for one year (Table S2, corrected). Comparing
functional diversity along different ecological gradients of
disturbances would make strong inference about impact of cat
predation on the functional structure of vertebrate communities,
but this is not feasible with citizen science data collected for
the 21 cats in this study. Functional diversity can be quantified
in several ways, with a myriad of functional diversity indices,
not only based on functional distances in multivariate space.
Some metrics were developed to quantify community assembly
processes. Metrics such as functional richness, have been shown
to correlate very well with ecosystem processes (Tilman et al.,
1997 and references thereof).
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Mori et al. Impacts of Free-Ranging Cats in Italy
Portions of functional space occupied by different classes were
compared using a convex hull approach. The convex hull is the
minimum convex geometry that includes all the observations
considered (Preparata and Shamos, 1985) and has recently been
proposed as a method for representing the volume of functional
space used by a community (Villéger et al., 2008). For each
prey class, we calculated the area of each convex hull. All
the analyses were carried in the software R (version 3.5.1., R
Foundation for Statistical Computing, Wien, Austria). The ape
package was used to perform the Principal Coordinate Analysis.
The code developed has been uploaded to a dedicated github
repository (https://github.com/drmarcogir/cats).
Variables Influencing Predation Rate by
Domestic Cats
We assessed the effect of five variables on the killing rate (i.e.,
number of prey brought home) by the 21 domestic cats that were
intensively monitored for 1 year through mixed effect models
computed in the R (version 3.5.1., R Foundation for Statistical
Computing, Wien, Austria) packages lme4 (Bates et al., 2014) and
MuMIn (Barton and Barton, 2015). The variables included in the
models were: latitude, distance from the countryside (measured
as the minimum distance from the house of the cat owner
and the border of human settlements, i.e., where the number
of houses inhabited by humans was <2/100 m2), duration of
cat outdoor activity (hours/day), presence/absence of a collar
with a bell (1 =present; 2 =absent), and sex (1 =male; 2 =
female). Bioclimatic ecoregions (cf. Blasi et al., 2014; Genovesi
et al., 2014) were included in the model as a random factor.
Before running the model, we tested for multicollinearity among
variables (i.e., r>|0.6|); no collinearity was detected among our
variables and, therefore, we included all of them in the total
model. Non-significant variables were removed one at a time
until the elimination of terms caused a significant increase in the
residual deviance.
RESULTS
Citizen Science Survey
We collected a total of 2042 entries for free-ranging vertebrates
killed by domestic cats (and 7 more killings of freshwater fish in
confined environments) (minimum number of cats, N=145;
number of owners, N=125) (Figure 2). Among those, 1,533
were killed in warm months (April–September). Our survey
was conducted throughout Italy, with data originating from 377
locations, including rural and urban areas, from sea level to
mountainous areas (Figure 2).
The prey killed belonged to at least 207 species (Table S3):
17.61% taxa (including fish, thus on the total list of Table
S2) were classified as “Threatened” or “Near Threatened”
by at least the Italian or the international IUCN Red Lists
and 7.77% as “Data Deficient” or “Not Evalutated” species
(Table 1;Table S3). Prey-species size ranged from 1 to 3
grams for juvenile amphibians to about 2 kg for subadult hares
and pheasants.
As to the 21 domestic cats (included among the
145 previously cited) that were followed for 1 year, the
FIGURE 2 | Locations of origin of our data, including rural areas (green-lined
circles) and urban centers (gray-bricked circles). Killings recorded far from
owner’s house (including those from smaller islands), i.e., with cats moving
with prey in their mouth, were not shown in this map.
predation rate showed considerable variation within and
among taxonomical classes. The most impacted classes
were mammals (40% of killings), followed by birds (35%),
reptiles (21%), and amphibians (4%). Over 73% of predations
occurred in spring and summer. A graphical summary
of total and within-class predation frequencies is shown
in Figure 3.
The most frequently killed species among mammals was
the house mouse Mus domesticus (10%), although Rattus rattus
(9.4%), Apodemus flavicollis (8.2%), Sciurus vulgaris (8.2%),
and Suncus etruscus (8.2%) were also reported many times:
all of these species are common species (“Least Concern”) in
Italy (Rondinini et al., 2013). As to birds, the most frequently
killed species were Turdus merula (13%), Passer italiae (7.9%),
Streptopelia decaocto (7.9%), and Sylvia atricapilla (7.9%); P.
italiae is endemic to Italy and is declining. In terms of reptiles,
the most frequently killed species were Podarcis muralis (29%),
Hierophis virdiflavus/carbonarius (12.8%), and Lacerta bilineata
(12.8%). Lastly, among amphibians, the most frequently killed
species were Rana dalmatina (40%) and Pelophylax synklepton
esculentus (20%), both listed within the annexes of the Habitat
Directive. A summary of the proportion of species killed by these
21 cats revealed that two out of the total of 207 are of conservation
concern (Figure 4): one amphibian and one bird species, Rana
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Mori et al. Impacts of Free-Ranging Cats in Italy
TABLE 1 | Near threatened, threatened, data deficient, and not evaluated prey species brought home by free-ranging domestic cats in Italy.
Class Order Species Number of individuals killed IUCN Red List Italian Red List
Birds Anseriformes Anas crecca 2 Least Concern Endangered
Birds Anseriformes Aythya ferina 1 Least Concern Endangered
Birds Charadriiformes Scolopax rusticola 6 Least Concern Data Deficient
Birds Charadriiformes Tringa erythropus 1 Least Concern Not Evaluated
Birds Columbiformes Streptopelia turtur 1 Vulnerable Least Concern
Birds Galliformes Alectoris rufa 3 Least Concern Data Deficient
Birds Galliformes Coturnix coturnix 5 Least Concern Data Deficient
Birds Gruiformes Crex crex 1 Least Concern Vulnerable
Birds Passeriformes Acrocephalus melanopogon 1 Least Concern Vulnerable
Birds Passeriformes Carduelis carduelis 19 Least Concern Near Threatened
Birds Passeriformes Carduelis chloris 22 Least Concern Near Threatened
Birds Passeriformes Delichon urbicum 4 Least Concern Near Threatened
Birds Passeriformes Emberiza schoeniclus 2 Least Concern Near Threatened
Birds Passeriformes Ficedula hypoleuca 3 Least Concern Not Evaluated
Birds Passeriformes Hirundo rustica 4 Least Concern Near Threatened
Birds Passeriformes Lanius collurio 2 Least Concern Vulnerable
Birds Passeriformes Passer italiae 79 Vulnerable Vulnerable
Birds Passeriformes Passer montanus 11 Least Concern Vulnerable
Birds Passeriformes Pyrrhula pyrrhula 1 Least Concern Vulnerable
Birds Passeriformes Saxicola rubicola 1 Least Concern Vulnerable
Birds Passeriformes Sylvia undata 1 Near Threatened Vulnerable
Birds Passeriformes Tarsiger cyanurus 1 Least Concern Not Evaluated
Birds Piciformes Jynx torquilla 2 Least Concern Endangered
Birds Strigiformes Asio flammeus 1 Least Concern Not Evaluated
Mammals Chiroptera Eptesicus serotinus 1 Least Concern Near Threatened
Mammals Chiroptera Miniopterus schreibersii 2 Near Threatened Least Concern
Mammals Chiroptera Myotis mystacinus 1 Least Concern Vulnerable
Mammals Chiroptera Myotis nattereri 1 Least Concern Vulnerable
Mammals Chiroptera Nyctalus leisleri 3 Least Concern Near Threatened
Mammals Chiroptera Pipistrellus nathusii 1 Least Concern Near Threatened
Mammals Chiroptera Plecotus auritus 1 Least Concern Near Threatened
Mammals Chiroptera Rhinolophus ferrumequinum 3 Near Threatened Vulnerable
Mammals Chiroptera Rhinolophus hipposideros 2 Near Threatened Vulnerable
Mammals Rodentia Apodemus alpicola 1 Least Concern Data Deficient
Mammals Rodentia Eliomys quercinus 3 Near Threatened Near Threatened
Mammals Soricomorpha Crocidura pachyura 4 Least Concern Data Deficient
Mammals Soricomorpha Sorex antinorii 16 Data Deficient Data Deficient
Mammals Soricomorpha Talpa caeca 2 Least Concern Data Deficient
Reptiles Squamata Anguis veronensis 10 Not Evaluated Least Concern
Reptiles Squamata Archaeolacerta bedriagae 1 Near Threatened Near Threatened
Reptiles Squamata Elaphe quatuorlineata 6 Near Threatened Least Concern
Reptiles Squamata Hierophis carbonarius 10 Not Evaluated Not Evaluated
Reptiles Squamata Malpolon monspessulanus 1 Least Concern Not Evaluated
Reptiles Squamata Podarcis filfolensis 12 Least Concern Vulnerable
Reptiles Squamata Podarcis tiliguerta 3 Least Concern Near Threatened
Reptiles Testudines Testudo hermanni 1 Near Threatened Endangered
Amphibia Anura Bufo bufo 2 Least Concern Vulnerable
Amphibia Anura Hyla arborea 4 Least Concern Not Evaluated
Amphibia Anura Rana latastei 1 Vulnerable Vulnerable
Amphibia Urodela Triturus carnifex 1 Least Concern Near Threatened
Predation rate by 21 cats followed for 1 year.
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Mori et al. Impacts of Free-Ranging Cats in Italy
FIGURE 3 | Reported killings of 21 domestic cats for the following groups of vertebrates: birds, mammals, reptiles, and amphibians. The thickness of black lines
represents the proportion of individuals of each killed species within each taxonomical class.
FIGURE 4 | Proportions of species killed by cats, grouped by threat
categories. The two panels show different groupings according to the IUCN
and Italian Red List species classifications. Legend codes indicate threat
categories: VU, Vulnerable; NT, Near Threatened; LC, Least Concern; DD,
Data Deficient; and NE, Not Evaluated. Alien species (i.e., those introduced to
Italy) were not classified according to the Red List categories.
latastei and Passer italiae, are classified as “Vulnerable” and one
reptile, Elaphe quatuorlineata, is classified as “Near Threatened”
by the IUCN Red List. In contrast, when grouping species
according to the Italian Red List, a further “Near Threatened”
amphibian (Triturus carnifex) and a “Vulnerable” bird (Pyrrhula
pyrrhula) were also included.
FIGURE 5 | Principal Coordinate Analysis (PCoA) performed on the trait matrix
of killed species. The ordination shows the distribution of different species
within trait space. Convex hulls, displayed in different colors, were calculated
for each taxonomic class.
When examining the diet in functional trait space, PCoA
analysis revealed that the class occupying the largest functional
space was birds, followed by mammals, reptiles, and amphibians
(Figure 5). Therefore, the largest impact was on the functional
structure of mammal and bird assemblages.
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Mori et al. Impacts of Free-Ranging Cats in Italy
TABLE 2 | Factors affecting the number of prey items brought home by domestic
cats in one year, estimated through a general linear model.
Variable B Standard error P
Distance from the countryside −0.04 0.01 <0.001**
Hours/day outside 0.95 0.24 <0.001**
Intercept 46.28 7.98 0.02*
Asterisks indicate significant P (*<0.05; ** <0.001).
Variables Influencing Killing Rates
The predation rate of the 21 individual cats followed for 1 year
increased with decreasing distance from the countryside and
increasing number of hours of outside activity per day (R2=0.92:
Table 2;Tables S4, S5).
DISCUSSION
Evidence of the effects of cat predation on wildlife are rare for
country-wide areas and generally comes from US urban and
suburban ecosystems, which are relatively poor in biodiversity
(e.g., Dunn and Tessaglia, 1993; Lepczyk et al., 2003; Loss et al.,
2013; Loss and Marra, 2017). The few European country-wide
studies on this topic are mostly taxon-specific (e.g., bats in Italy:
Ancillotto et al., 2013, 2019; Siberian chipmunks: Mori et al.,
2018). The only general study carried out in continental Europe
(Poland) showed that free-ranging domestic cats mainly prey
on wild mammals (Krauze-Gryz et al., 2012), but this study
was limited to a very few rural areas. Conversely, our survey
was conducted throughout Italy, both in rural areas and urban
centers, from sea level to the mountains. The Mediterranean
basin (i.e., northern Africa, the Middle East, and southern
Europe, including the whole of Italy) is included in a biodiversity
hotspot, i.e., one of the world’s 36 biogeographic regions with
significant levels of biodiversity, which is threatened by human
activities (Noss et al., 2015). Introduced species, including feral
ones, represent one of the main causes of biodiversity crisis,
particularly in these areas (Wonham, 2006). Our analysis showed
that at least 207 species, ranging in size from juvenile neo-
metamorphosed frogs to adult weasels and hares, may be actively
killed by free-ranging domestic cats. Over 30 of these are listed
as “Threatened” by the International Red list, whereas the great
majority (i.e., over 75%) of species killed by free-ranging cats
belong to the “Least Concern” category. This is consistent
with the fact that Least Concern species are—on average—the
most abundant species and thus potentially the most available
to domestic cats, which are opportunistic predators (Loss and
Marra, 2017). However, despite their widespread distribution and
presence, these species may play key roles in the maintenance of
other carnivore species deserving conservation measures, whose
diet is based precisely on the species killed by domestic cats (e.g.,
Bertolino et al., 2015), and this may suggest a strong role for cat
predations in ecosystem functioning. Moreover, the few reported
kills of threatened species may be more deleterious than for many
of the common widespread species. The Italian sparrow, Passer
italiae, is endemic to Italy and is classified as “Vulnerable.” The
high predation rate by domestic cats on this bird may therefore
be a threat to its conservation. Other endemic/near endemic
Italian species that are highly preyed upon by domestic cats in
Italy include the Valais shrew, Sorex antinorii, classified as “Data
Deficient,” the Sicilian shrew, Crocidura sicula, and the Italian
slow worm, Anguis veronensis. Italy plays a key role in Europe
in the conservation of the Eurasian red squirrel, Sciurus vulgaris,
which is threatened by habitat fragmentation and competition
with introduced species (Bertolino and Genovesi, 2003; Bertolino
et al., 2015); this rodent is among the main species killed by
domestic cats (i.e., over 8% predations). Moreover, we confirmed
that free-roaming domestic cats may represent a huge threat to
bat assemblages (Ancillotto et al., 2013), which include a number
of imperiled species representing paramount bioindicators of
environmental quality (Jones et al., 2009).
Free-ranging domestic cats may be active throughout the
day and the night (Cove et al., 2018), therefore potentially
affecting spatiotemporal behavior and the abundance of diurnal
and nocturnal species (Parsons et al., 2018). Accordingly, the
daily number of hours of a cat outside activity significantly
increased the number of prey killed by cats. Furthermore, their
home range size may exceed 10 hectares, even in urban areas
(Pillay et al., 2018), and covering even larger areas in rural
environments (up to 228 hectares, in male cats: Tschanz et al.,
2011; Loss et al., 2013). Distance from the countryside was found
to affect the number of prey items brought home by cats per
year. This is in line with the longer distances traveled by free-
ranging cats in these areas. Conversely, we detected no effect of
the local climatic ecoregion (cf. Blasi et al., 2014) nor of the sex
of the cat on the predation rate, despite intersexual differences
in hunting ability that occur in this species. Additionally, the
presence of a bell on the collar of the cat was not effective
in reducing wildlife killings, in contrast with anecdotal report
by cat owners (unpublished data) and despite reports that, on
islands, bells may reduce predations on birds (Calver et al., 2007;
Gordon et al., 2010). Cat bibs are neoprene triangular pieces
of brightly colored plastic material attached to cat collars that
are used on free-roaming cats to warn possible prey of the
presence of the cat, reducing their probability of being killed.
However, although potentially functional in reducing predation,
cat bibs did not eliminate predation on wildlife by domestic cats
(van Heezik, 2010).
The wide ecological plasticity of domestic cats supports
the fact that the domestic cat is on the “100 of the world’s
worst invasive alien species” list, with populations increasing
worldwide and in a huge variety of habitat types (Loss and
Marra, 2017; Pillay et al., 2018). In this paper, we did not
estimate the population abundance of killed species, so we
cannot describe any impacts at the population level. However,
we provided evidence that the strongest impact of domestic cats
occurs at the functional structure level of mammal and bird
assemblages (Lepczyk et al., 2003; Siracusa, 2010; Bonnington
et al., 2013). Domestic cats are apex predators that show at
least two reproductive peaks per year (Sogliani and Mori,
2019); thus, they may have few competitors (Castañeda et al.,
2018; Sogliani and Mori, 2019) and may rapidly become the
most abundant carnivorous species (Loss et al., 2013). Having
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Mori et al. Impacts of Free-Ranging Cats in Italy
population densities of all prey species throughout all study area
would have allowed us to calculate killed prey selection, i.e.,
by comparing the total individual killed per species (i.e., the
predation pressure) on the total population size for each species.
Unfortunately, data on population density in the wild are limited
particularly for small species such as reptiles, amphibians, non-
migrant small birds and small mammals. The largest database
of vertebrate abundance (Santini et al., 2018) only includes
estimates of population density for 41 species and in few localities
per species: in Italy there are over 780 species of terrestrial
vertebrates, many of which live in hundreds localities. We are
aware that our dataset is far from being complete, as confirmed
by other species killed by cats outside our sampling period (the
little bittern in 2019; the Bechstein’s bat in 2013: Ancillotto et al.,
2013); moreover we sampled a limited percentage of Italian free-
ranging cats (and the number of prey killed by a cat in one year
is only available for 21 cats). Therefore, as to the precautionary
principle (Khayat et al., 2020), we are confident that impact occur
particularly on K-strategy species (e.g., nocturnal mammals such
as bats bats: Khayat et al., 2020) or species linked to transient
habitats (e.g., Amphibians, crossing roads at night) and limited
areas (e.g., islands), even if killed only occasionally. A high
number of killings would also affect populations of Least Concern
species, which represent indeed the majority of killings, possibly
due to their abundance, particularly if exerted by a non-native
predator such as the domestic cat. Further research is needed to
assess the actual local effect at population levels.
Reducing the impacts of invasive species on wildlife requires
eradication or at least reduction in population size through
sterilization. Both of these strategies are often blocked by the
general public, particularly when involving charismatic fauna
(e.g., Bertolino and Genovesi, 2003; Crowley et al., 2017, 2018,
2019a). Reproduction control (i.e., sterilization) is reported to
be a good way to control and manage urban populations of
domestic cats, i.e., where human density is the highest and
where eradication projects are mostly boycotted (Natoli et al.,
2006). In rural areas, veterinarians who frequently deal with pet
owners should encourage sterilization, using cat welfare as the
main argument to convince cat owners (cf. Grayson and Calver,
2004). Sterilization would not prevent predation of wildlife by
domestic cats, but it limits the number of offspring and thus
the population size (Jones and Downs, 2011). For ethical reasons
and considering the widespread denial of the negative impacts
of domestic cats in western countries (Loss et al., 2018; Crowley
et al., 2019b), lethal control would be challenging (Natoli et al.,
2006; Thomas et al., 2013).
Citizen science has been proven to be effective in collecting
data involving feral pets. Therefore, we suggest that it could
be used as a tool to lead cat owners toward responsible
ownership, e.g., through social media campaigns and public
divulgation/discussion events in the main urban areas and
meeting points. We strongly recommend cat owners to keep
their pet cats indoors or, at least, limit their ranging bouts by
avoiding nocturnal and crepuscular hours, particularly in warm
months, i.e., when most wild species are active and in their
reproductive periods. Together, the effectiveness of cat bibs for
reducing predation on wildlife should be statistically tested (van
Heezik, 2010). Field studies like this one may provide a scientific
basis on which to build well-supported dissemination campaigns
to fight against misinformation on this topic and, more generally,
on the impacts of biological invasions (Natoli et al., 2006; Loss
et al., 2018). However, scientific articles are unlikely to change
the behavior of pet owners per se. Given the full-blown denial of
the negative impacts of cats, which is also supported by published
position papers (Lynn et al., 2019), the behavior of cat owners
might be difficult to change, even in a biodiversity hotspot such
as the Mediterranean basin. Cat welfare, including the increased
risk of disease contraction in free-roaming individuals (Frenkel
et al., 1970; Slater, 2004) and predation by wild carnivores
(Sogliani and Mori, 2019), should thus be considered as effective
methods to encourage cat owners to keep domestic cats under
controlled conditions (McDonald et al., 2015). Laws state that
it is a misdemeanor offense to not provide cats with adequate
food, shelter, and freedom from pain, preventing cruelty but
also promoting responsible cat ownership. Keeping cats indoors
would help prevent damage to native wildlife and the spread
of diseases and zoonoses from wild species to domestic cats.
Increased inter- and intra-specific competition would increase
cat stress: responsible owners should alleviate stress by reducing
the encounters between cats and other species/individuals, as well
as by taking care of their health status.
DATA AVAILABILITY STATEMENT
The datasets used for analysis in this study can be found in online
repositories [https://github.com/drmarcogir/cats]. Photos,
sensitive data and coordinates of owner’s houses analyzed in this
study are subject to the following licenses/restrictions [National
Law 633/1941 and following integrations, DL 196/2003;
General Data Protection Regulation – EU Regulation 2016/679]
and cannot be shared also in line with assurance provided
to citizen-scientists.
AUTHOR CONTRIBUTIONS
EM and MM: conceptualization. KT, AC, and LC: data collection.
EM: supervision. MG: methodology. EM, MM, and MG:
writing—original draft. All authors: review and editing.
ACKNOWLEDGMENTS
Authors would like to thank L. Ancillotto and all of the cat owners
who provided data. We thank I. Kay-Lavelle, V. Sfondrini,
and E. Bassett for language revision. Four reviewers and the
Associate Editor, Franco Andreone, improved our first draft with
their comments.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/fevo.
2019.00477/full#supplementary-material
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Mori et al. Impacts of Free-Ranging Cats in Italy
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Conflict of Interest: The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be construed as a
potential conflict of interest.
The reviewer GB declared a past co-authorship with one of the authors, EM
to the handling editor.
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Girardello. This is an open-access article distributed under the terms of the Creative
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