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
Frontiers in Ecology and Evolution | www.frontiersin.org 2December 2019 | Volume 7 | Article 477

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
Mammal and bird trait data (i.e., body mass and diet: Table S2)
were derived from a comprehensive database, including species-
level trait data for all bird and mammal species, taken from key
literature sources (Wilman et al., 2014). The traits of reptiles were
taken from Grimm et al. (2014), whereas those of amphibians
were derived from Trochet et al. (2014). Further published works
used to derive the traits of reptiles and amphibians (i.e., body
mass and diet) are shown in Table S2. We investigated traits
by measuring (i) the quantity of resources consumed and (ii)
body mass, for a total of 11 traits (see Table S2). Trait data
for all of the killed species classes were pooled together into a
single matrix. We used Principal Coordinate Analysis (hereafter,
PCoA) to summarize the major patterns of variation in the
Frontiers in Ecology and Evolution | www.frontiersin.org 3December 2019 | Volume 7 | Article 477

Mori et al. Impacts of Free-Ranging Cats in Italy
resultant trait matrix (Legendre and Legendre, 2012). The main
advantage of this method is that it can use different dissimilarity
matrices from traditional ordination techniques, e.g., Principal
Component Analysis (PCA) (Legendre and Legendre, 2012). We
used the Gower general dissimilarity index (Gower, 1971) and a
distance matrix, as the input matrix contained both continuous
and categorical variables.
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 vertebrates killed by
domestic cats (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):
75.8% were classified as “Least Concern” by both the IUCN and
Italian Red Lists, 16.4% were “Near Threatened” or “Threatened,”
and the remaining 7.8% included “Data Deficient” or “Not
FIGURE 2 | Locations of origin of our data, including rural areas (green-lined
circles) and urban centers (gray-bricked circles).
Evaluated” 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 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
Frontiers in Ecology and Evolution | www.frontiersin.org 4December 2019 | Volume 7 | Article 477

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.
Frontiers in Ecology and Evolution | www.frontiersin.org 5December 2019 | Volume 7 | Article 477

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.
these 21 cats revealed that two out of the total of 207 are of
conservation concern (Figure 4): one amphibian species, Rana
latastei, is classified as “Vulnerable,” and one reptile, Elaphe
quatuorlineata, is classified as “Near Threatened” by the IUCN
Red List. In contrast, when grouping the species according to the
Italian Red List, they included six “Near Threatened” birds and
one “Vulnerable” amphibian species.
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.
Frontiers in Ecology and Evolution | www.frontiersin.org 6December 2019 | Volume 7 | Article 477

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).
Frontiers in Ecology and Evolution | www.frontiersin.org 7December 2019 | Volume 7 | Article 477

Mori et al. Impacts of Free-Ranging Cats in Italy
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
All datasets generated for this study are included in the
article/Supplementary Material.
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
REFERENCES
Ancillotto, L., Serangeli, M. T., and Russo, D. (2013). Curiosity killed
the bat: domestic cats as bat predators. Mammal. Biol. 78, 369–373.
doi: 10.1016/j.mambio.2013.01.003
Ancillotto, L., Venturi, G., and Russo, D. (2019). Presence of humans
and domestic cats affects bat behaviour in an urban nursery of greater
horseshoe bats (Rhinolophus ferrumequinum). Behav. Proc. 164, 4–9.
doi: 10.1016/j.beproc.2019.04.003
Barton, K., and Barton, M. K. (2015). Package ‘MuMIn’.
R package version.
Bassi, E., Canu, A., Firmo, I., Mattioli, L., Scandura, M., and Apollonio,
M. (2017). Trophic overlap between wolves and free-ranging wolf×dog
hybrids in the Apennine Mountains, Italy. Glob. Ecol. Cons. 9, 39–49.
doi: 10.1016/j.gecco.2016.11.002
Bates, D., Maechler, M., Bolker, B., and Walker, S. (2014). lme4: Linear
mixed-effects models using Eigen and S4. R Pack. Vers. 1, 1–23.
doi: 10.18637/jss.v067.i01
Bertolino, S., Colangelo, P., Mori, E., and Capizzi, D. (2015). Good for
management, not for conservation: an overview of research, conservation
and management of Italian small mammals. Hystrix 26, 25–35.
doi: 10.4404/hystrix-26.1-10263
Bertolino, S., and Genovesi, P. (2003). Spread and attempted eradication
of the grey squirrel (Sciurus carolinensis) in Italy, and consequences for
the red squirrel (Sciurus vulgaris) in Eurasia. Biol. Cons. 109, 351–358.
doi: 10.1016/S0006-3207(02)00161-1
Birò, Z., Lanszki, J., Szemethy, L., Heltai, M., and Randi, E. (2005). Feeding habits
of feral domestic cats (Felis catus), wild cats (Felis silvestris) and their hybrids:
trophic niche overlap among cat groups in Hungary. J. Zool. 266, 187–196.
doi: 10.1017/S0952836905006771
Frontiers in Ecology and Evolution | www.frontiersin.org 8December 2019 | Volume 7 | Article 477

Mori et al. Impacts of Free-Ranging Cats in Italy
Blackburn, T. M., Cassey, P., Duncan, R. P., Evans, K. L., and Gaston, K. J. (2004).
Avian extinction and mammalian introductions on oceanic islands. Science 305,
1955–1958. doi: 10.1126/science.1101617
Blasi, C., Capotorti, G., Copiz, R., Guida, D., Mollo, B., Smiraglia, D., et al.
(2014). Classification and mapping of the ecoregions of Italy. Plant Biosyst. 148,
1255–1345. doi: 10.1080/11263504.2014.985756
Boano, G., Perco, F., Pavia, M. and Baldaccini, N. E. (2019). Columba livia
domestic breed, invasive entity also alien for Italy. Riv. Ital. Ornitol. 88, 3–10.
doi: 10.4081/rio.2018.356
Bonnaud, E., Bourgeois, K., Vidal, E., Legrand, J., and Le Corre, M.
(2009). How can the Yelkouan shearwater survive feral cat predation?
A meta-population structure as a solution? Popul. Ecol. 51, 261–270.
doi: 10.1007/s10144-008-0134-0
Bonnaud, E., Medina, F. M., Vidal, E., Nogales, M., Tershy, B., Zavaleta, E., et al.
(2011). The diet of feral cats on islands: a review and a call for more studies.
Biol. Invasions 13, 581–603. doi: 10.1007/s10530-010-9851-3
Bonnington, C., Gaston, K. J., and Evans, K. L. (2013). Fearing the feline:
domestic cats reduce avian fecundity through trait-mediated indirect effects
that increase nest predation by other species. J. Appl. Ecol. 50, 15–24.
doi: 10.1111/1365-2664.12025
Calver, M., Thomas, S., Bradley, S., and McCutcheon, H. (2007). Reducing the
rate of predation on wildlife by pet cats: the efficacy and practicability
of collar-mounted pounce protectors. Biol. Cons. 137, 341–348.
doi: 10.1016/j.biocon.2007.02.015
Carthey, A. J., and Banks, P. B. (2012). When does an alien become a
native species? A vulnerable native mammal recognizes and responds to
its long-term alien predator. PLoS ONE 7:e31804. doi: 10.1371/journal.pone.
0031804
Castañeda, I., Bellard, C., Jari,´
c, I., Pisanu, B., Chapuis, J. L., and Bonnaud,
E. (2018). Trophic patterns and home-range size of two generalist
urban carnivores: a review. J. Zool. 307, 79–82. doi: 10.1111/jzo.
12623
Cilleros, K., Allard, L., Grenouillet, G., and Brosse, S. (2016). Taxonomic and
functional diversity patterns reveal different processes shaping European
and Amazonian stream fish assemblages. J. Biogeogr. 43, 1832–1843.
doi: 10.1111/jbi.12839
Cove, M. V., Gardner, B., Simons, T. R., Kays, R., and O’Connell, A. F.
(2018). Free-ranging domestic cats (Felis catus) on public lands: estimating
density, activity, and diet in the Florida Keys. Biol. Invasions 20, 333–344.
doi: 10.1007/s10530-017-1534-x
Crowley, S. L., Cecchetti, M., and McDonald, R. A. (2019b). Hunting behaviour in
domestic cats: an exploratory study of risk and responsibility among cat owners.
People Nat. 1, 18–30 doi: 10.1002/pan3.6
Crowley, S. L., Hinchliffe, S., and McDonald, R. A. (2017). Invasive species
management will benefit from social impact assessment. J. Appl. Ecol. 54,
351–357. doi: 10.1111/1365-2664.12817
Crowley, S. L., Hinchliffe, S., and McDonald, R. A. (2018). Killing squirrels:
exploring motivations and practices of lethal wildlife management. Environ.
Plann. E Nat. Space 1, 120–143. doi: 10.1177/2514848617747831
Crowley, S. L., Hinchliffe, S., and McDonald, R. A. (2019a). The Parakeet
Protectors: understanding opposition to introduced species management. J.
Env. Manage. 229, 120–132. doi: 10.1016/j.jenvman.2017.11.036
Davis, A. J., Huijbregts, H., and Krikken, J. (2000). The role of local and regional
processes in shaping dung beetle communities in tropical forest plantations in
Borneo. Glob. Ecol. Biogeog. 9, 281–292. doi: 10.1046/j.1365-2699.2000.00189.x
Davison, A., Birks, J. D. S., Griffiths, H. I., Kitchener, A. C., Biggins, D.,
and Butlin, R. K. (1999). Hybridization and the phylogenetic relationship
between polecats and domestic ferrets in Britain. Biol. Cons. 87, 155–161.
doi: 10.1016/S0006-3207(98)00067-6
Doherty, T. S., Dickman, C. R., Glen, A. S., Newsome, T. M., Nimmo, D. G.,
Ritchie, E. G., et al. (2017). The global impacts of domestic dogs on threatened
vertebrates. Biol. Conserv. 210, 56–59. doi: 10.1016/j.biocon.2017.04.007
Doherty, T. S., Glen, A. S., Nimmo, D. G., Ritchie, E. G., and Dickman, C. R. (2016).
Invasive predators and global biodiversity loss. Proc. Nat. Ac. Sci. U.S.A. 113,
11261–11265. doi: 10.1073/pnas.1602480113
Dunn, E. H., and Tessaglia, D. L. (1993). Predation of birds at feeders in winter. J.
Field Ornithol. 65, 8–16.
Faulquier, L., Fontaine, R., Vidal, E., Salamolard, M., and Le Corre, M. (2009). Feral
cats Felis catus threaten the endangered endemic Barau’s petrel Pterodroma
baraui at Reunion Island (Western Indian Ocean). Waterbirds 32, 330–336.
doi: 10.1675/063.032.0213
Fitzgerald, B. M., and Turner, D. C. (2000). “Hunting behaviour of domestic cats
and their impact on prey populations,” in The Domestic Cat: The Biology of Its
Behaviour, 2nd edn, eds D. C. Turner, and P. Bateson (Cambridge: Cambridge
University Press), 148–171.
Flux, J. E. C., and Fullagar, P. J. (1992). World distribution of the
Rabbit Oryctolagus cuniculus on islands. Mammal Rev. 22, 151–205.
doi: 10.1111/j.1365-2907.1992.tb00129.x
Frank, A. S., Carthey, A. J., and Banks, P. B. (2016). Does historical coexistence
with dingoes explain current avoidance of domestic dogs? Island bandicoots
are naïve to dogs, unlike their mainland counterparts. PloS ONE 11:e0161447.
doi: 10.1371/journal.pone.0161447
Frenkel, J. K., Dubey, J. P., and Miller, N. L. (1970). Toxoplasma gondii
in cats: fecal stages identified as coccidian oocysts. Science 167, 893–896.
doi: 10.1126/science.167.3919.893
Genovesi, P., Angelini, P., Dupr,è, E., Ercole, S., Giacanelli, V., Ronchi, F., et al.
(2014). Specie ed habitat di interesse comunitario in Italia: Distribuzione, Stato
di Conservazione e Trend. Roma: ISPRA, Serie Rapporti.
Gillies, C. (2001). Advances in New Zealand Mammalogy 1990–2000: house
cat. J. Royal Soc. New Zeal. 31, 205–218. doi: 10.1080/03014223.2001.
9517648
Gordon, J. K., Matthaei, C., and Van Heezik, Y. (2010). Belled collars reduce
catch of domestic cats in New Zealand by half. Wildl. Res. 37, 372–378.
doi: 10.1071/WR09127
Gower, J. C. (1971). A general coefficient of similarity and some of its properties.
Biometrics 1, 857–871. doi: 10.2307/2528823
Grayson, J., and Calver, M. C. (2004). Regulation of domestic cat ownership
to protect urban wildlife: a justification based on the precautionary
principle. Royal Zool. Soc. New South Wales 1, 169–178. doi: 10.7882/FS.20
04.094
Green, J. S., and Gipson, P. S. (1994). “Feral dogs,” in The handbook: Prevention
and Control of Wildlife Damage, eds Internet Center for Wildlife Damage
Management, 35, (Lincoln, NE: University of Nebraska Editions).
Grimm, A., Ramirez, A. M. P., Moulherat, S., Reynaud, J., and Henle, K. (2014).
Life-history database of European reptile species. Nature Cons. 9, 45–67.
doi: 10.3897/natureconservation.9.8908
Hall, C. M., Adams, N. A., Bradley, J. S., Bryant, K. A., Davis, A. A., Dickman,
C. R., et al. (2016). Community attitudes and practices of urban residents
regarding predation by pet cats on wildlife: an international comparison. PLoS
ONE 11:e0151962. doi: 10.1371/journal.pone.0151962
Harper, G.A. (2005). Numerical and functional response of feral cats (Felis catus)
to variations in abundance of primary prey on Stewart Island (Rakiura), New
Zealand. Wildl. Res. 32, 597–604. doi: 10.1071/WR04057
Hejda, M., Pyšek, P., and Jarosik, V. (2009). Impact of invasive plants on the
species richness, diversity and composition of invaded communities. J. Ecol.
97, 393–403. doi: 10.1111/j.1365-2745.2009.01480.x
Hinshaw, V. S., Webster, R. G., and Turner, B. (1978). Novel Influenza A
viruses isolated from Canadian feral ducks: including strains antigenically
related to swine influenza (Hsw1N1) viruses. J. Gen. Virol. 41, 115–127.
doi: 10.1099/0022-1317-41-1-115
Home, C., Bhatnagar, Y. V., and Vanak, A. T. (2017). Canine Conundrum:
domestic dogs as an invasive species and their impacts on wildlife in India.
Anim. Cons. 21, 275–282. doi: 10.1111/acv.12389
Hughes, B. J., Martin, G. R., and Reynolds, S. J. (2008). Cats and seabirds: effects
of feral domestic cat Felis silvestris catus eradication on the population of
sooty terns Onychoprion fuscata on Ascension Island, South Atlantic. Ibis 150,
122–131. doi: 10.1111/j.1474-919X.2008.00838.x
Hughes, J., and Macdonald, D. W. (2013). A review of the interactions
between free-roaming domestic dogs and wildlife. Biol. Cons. 157, 341–351.
doi: 10.1016/j.biocon.2012.07.005
Jones, A. L., and Downs, C. T. (2011). Managing feral cats on a university’s
campuses: how many are there and is sterilization having an effect?
J. Appl. Anim. Welfare Sci. 14, 304–320. doi: 10.1080/10888705.2011.
600186
Frontiers in Ecology and Evolution | www.frontiersin.org 9December 2019 | Volume 7 | Article 477

Mori et al. Impacts of Free-Ranging Cats in Italy
Jones, G., Jacobs, D. S., Kunz, T. H., Willig, M. R., and Racey, P. A. (2009). Carpe
noctem: the importance of bats as bioindicators. Endang. Spec. Res. 8, 93–115.
doi: 10.3354/esr00182
Keitt, B. S., Wilcox, C., Tershy, B. R., Croll, D. A., and Donlan, C. J. (2002).
The effect of feral cats on the population viability of black-vented shearwaters
(Puffinus opisthomelas) on Natividad Island, Mexico. Anim. Cons. 5, 217–223.
doi: 10.1017/S1367943002002263
Krauze-Gryz, D., Gryz, J., and Goszczynski, J. (2012). Predation by
domestic cats in rural areas of central Poland: an assessment based
on two methods. J. Zool. 288, 260–266. doi: 10.1111/j.1469-7998.2012.
00950.x
Kutt, A. S. (2012). Feral cat (Felis catus) prey size and selectivity in north-
eastern Australia: implications for mammal conservation. J. Zool. 287, 292–300.
doi: 10.1111/j.1469-7998.2012.00915.x
Legendre, P., and Legendre, L. (2012). Numerical Ecology. London:
Elsevier Editions.
Lepczyk, C. A., Mertig, A. G., and Liu, J. (2003). Landowners and cat
predation across rural-to-urban landscapes. Biol. Cons. 115, 191–201.
doi: 10.1016/S0006-3207(03)00107-1
Liberg, O. (1984). Food habits and prey impact by feral and house-based
domestic cats in a rural area in Southern Sweden. J. Mammal. 65, 424–432.
doi: 10.2307/1381089
Loss, S. R., and Marra, P. P. (2017). Population impacts of free-ranging
domestic cats on mainland vertebrates. Front. Ecol. Environm. 15, 502–509.
doi: 10.1002/fee.1633
Loss, S. R., Will, T., Longcore, T., and Marra, P. P. (2018). Responding to
misinformation and criticisms regarding United States cat predation
estimates. Biol. Invasions 20, 3385–3396. doi: 10.1007/s10530-018-
1796-y
Loss, S. R., Will, T., and Marra, P. P. (2013). The impact of free-ranging
domestic cats on wildlife of the United States. Nat. Comm. 4:1936.
doi: 10.1038/ncomms2380
Lynn, W. S., Santiago-Ávila, F., Lindenmayer, J., Hadidian, J., Wallach, A., and
King, B. J. (2019). A moral panic over cats. Conserv. Biol. 33, 769–776.
doi: 10.1111/cobi.13346
Maiorano, L., Falcucci, A., Garton, E. O., and Boitani, L. (2007). Contribution of
the Natura 2000 network to biodiversity conservation in Italy. Cons. Biol. 21,
1433–1444. doi: 10.1111/j.1523-1739.2007.00831.x
Malo, J. E., Acebes, P., Giannoni, S. M., and Traba, J. (2011). Feral livestock
threatens landscapes dominated by columnar cacti. Acta Oecol. 37, 249–255.
doi: 10.1016/j.actao.2011.02.008
Mazel, F., Wüest, R. O., Lessard, J. P., Renaud, J., Ficetola, G. F., Lavergne, S.,
et al. (2017). Global patterns of β-diversity along the phylogenetic time-scale:
The role of climate and plate tectonics. Glob. Ecol. Biogeog. 26, 1211–1221.
doi: 10.1111/geb.12632
McDonald, J. L., Maclean, M., Evans, M. R., and Hodgson, D. J. (2015). Reconciling
actual and perceived rates of predation by domestic cats. Ecol. Evol. 5,
2745–2753. doi: 10.1002/ece3.1553
Medina, F. M., Bonnaud, E., Vidal, E., Tershy, B. R., Zavaleta, E. S., Josh
Donlan, C., et al. (2011). A global review of the impacts of invasive
cats on island endangered vertebrates. Glob. Change Biol. 17, 3503–3510.
doi: 10.1111/j.1365-2486.2011.02464.x
Medina, F. M., and Garcìa, R. (2007). Predation of insects by feral cats (Felis
silvestris catus L., 1758) on an oceanic island (La Palma, Canary Island). J. Insect
Conserv. 11, 203–207. doi: 10.1007/s10841-006-9036-7
Meek, P. D. (1998). Food items brought home by domestic cats Felis catus (L)
living in Booderee National Park, Jervis Bay. Proc. Linn. Soc. New South Wales
120, 43–47.
Mori, E., Zozzoli, R., and Menchetti, M. (2018). Global distribution and status of
introduced Siberian chipmunks Eutamias sibiricus.Mammal Rev. 48, 139–152.
doi: 10.1111/mam.12117
Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A., and Kent, J.
(2000). Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
doi: 10.1038/35002501
Natoli, E. (1994). Urban feral cats (Felis catus L.): perspectives for a demographic
control respecting the psycho-biological welfare of the species. Ann. Ist Sup.
Sanità 30, 223–227.
Natoli, E., Marigliano, L., Cariola, G., Faini, A., Bonanni, R., Cafazzo, S., et al.
(2006). Management of feral domestic cats in the urban environment of
Rome (Italy). Prev. Vet. Med. 77, 180–185. doi: 10.1016/j.prevetmed.2006.
06.005
Noss, R. F., Platt, W. J., Sorrie, B. A., Weakley, A. S., Means, D. B., Costanza,
J., et al. (2015). How global biodiversity hotspots may go unrecognized:
lessons from the North American Coastal Plain. Divers. Distrib. 21, 236–244.
doi: 10.1111/ddi.12278
Oliver, T. H., Heard, M. S., Isaac, N. J. B., Roy, D. B., Procter, D., Eigenbrod, F.,
et al. (2015). Biodiversity and resilience of ecosystem functions. Trends Ecol.
Evol. 30, 673–684. doi: 10.1016/j.tree.2015.08.009
Oosterbroek, P. (1994). Biodiversity of the Mediterranean region. Syst. Assoc.
50, 289–289.
Parsons, M. H., Banks, P. B., Deutsch, M. A., and Munshi-South, J. (2018).
Temporal and space-use changes by rats in response to predation by feral cats
in an urban ecosystem. Front. Ecol. Evol. 6:146. doi: 10.3389/fevo.2018.00146
Pearre, S., and Maass, R. (1998). Trends in the prey size-based trophic
niches of feral and house cats Felis catus L. Mammal Rev. 28, 125–139.
doi: 10.1046/j.1365-2907.1998.00030.x
Pillay, K. R., Streicher, J., and Downs, C. T. (2018). Home range and habitat use
of feral cats in an urban mosaic in Pietermaritzburg, KwaZulu-Natal, South
Africa. Urb. Ecosyst. 5, 999–1009. doi: 10.1007/s11252-018-0766-6
Preparata, F. P., and Shamos, M. I. (1985). Computational geometry. Texts and
Monographs in Computer Science. New York, NY: Springer-Verlag Editions.
doi: 10.1007/978-1-4612-1098-6
Randi, E., Pierpaoli, M., Beaumont, M., Ragni, B., and Sforzi, A. (2001).
Genetic identification of wild and domestic cats (Felis silvestris) and
their hybrids using Bayesian clustering methods. Mol. Ecol. 17, 285–293.
doi: 10.1111/j.1365-294X.2007.03417.x
Rondinini, C., Battistoni, A., Peronace, V., and Teofili, C. (2013). Lista Rossa
IUCN dei Vertebrati Italiani. Rome: Comitato Italiano IUCN e Ministero
dell’Ambiente e della Tutela del Territorio e del Mare.
Sanders, N. J., Gotelli, N. J., Heller, N. E., and Gordon, D. M. (2003). Community
disassembly by an invasive species. Proc. Nat. Ac. Sci. U.S.A. 100, 2474–2477.
doi: 10.1073/pnas.0437913100
Scott, M. D., and Causey, K. (1973). Ecology of feral dogs in Alabama. J. Wildl.
Manage. 37, 253–265. doi: 10.2307/3800116
Siracusa, A. M. (2010). Relazione tra una comunità di uccelli e densità di gatto
domestico Felis silvestris catus in un’area urbana siciliana. Avocetta 34, 57–61.
Slater, M. R. (2004). Understanding issues and solutions for unowned,
free-roaming cat populations. J. Am. Vet. Med. Assoc. 225, 1350–1354.
doi: 10.2460/javma.2004.225.1350.1
Sogliani, D., and Mori, E. (2019). “The Fox and the Cat”: sometimes they do not
agree. Mammal. Biol. 95: 150–154. doi: 10.1016/j.mambio.2018.07.003
Széles, G. L., Purger,J. J., Molnár, T., and Lanszki, J. (2018). Comparative analysis of
the diet of feral and house cats and wildcat in Europe. Mammal Res. 63, 43–53.
doi: 10.1007/s13364-017-0341-1
Thomas, R. L., Fellowes, M. D., and Baker, P. J. (2013). Spatio-temporal
variation in predation by urban domestic cats (Felis catus) and the
acceptability of possible management actions in the UK. PLoS ONE 7:e49369.
doi: 10.1371/journal.pone.0049369
Tilman, D., Knops, J., Wedin, D., Reich, P., Ritchie, M., and Siemann, E. (1997).
The influence of functional diversity and composition on ecosystem processes.
Science 277, 1300–1302. doi: 10.1126/science.277.5330.1300
Trochet, A., Moulherat, S., Calvez, O., Stevens, V. M., Clobert, J., and Schmeller,
D. S. (2014). A database of life-history traits of European amphibians. Biodiv.
Data J. 2:e4123. doi: 10.3897/BDJ.2.e4123
Tschanz, B., Hegglin, D., Gloor, S., and Bontadina, F. (2011). Hunters and non-
hunters: skewed predation rate by domestic cats in a rural village. Eur. J. Wildl.
Res. 57, 597–602. doi: 10.1007/s10344-010-0470-1
van Heezik, Y. (2010). Pussyfooting around the issue of cat predation in urban
areas. Oryx 44, 153–154. doi: 10.1017/S003060531000027X
Van’t Woudt, B. D. (1990). Roaming, stray, and feral domestic cats and dogs as
wildlife problems. Proc. 14th Vertebr. Pest Conf. 78, 291–295.
Villéger, S., Mason, N. W., and Mouillot, D. (2008). New multidimensional
functional diversity indices for a multifaceted framework in functional ecology.
Ecology 89, 2290–2301. doi: 10.1890/07-1206.1
Frontiers in Ecology and Evolution | www.frontiersin.org 10 December 2019 | Volume 7 | Article 477

Mori et al. Impacts of Free-Ranging Cats in Italy
Wilman, H., Belmaker, J., Simpson, J., de la Rosa, C., Rivadeneira, M.
M., and Jetz, W. (2014). EltonTraits 1.0: Species-level foraging attributes
of the world’s birds and mammals. Ecol. 95:2027. doi: 10.1890/13-
1917.1
Wonham, M. (2006). “Species invasions,” in Principles of Conservation Biology,
eds M. J. Groom, G. K. Meffe, and C. R. Carroll (Sunderland, MA: Sinauer
Associates Editions), 209–227.
Woods, M., McDonald, R. A., and Harris, S. (2003). Predation of wildlife
by domestic cats Felis catus in Great Britain. Mammal Rev. 33, 174–188.
doi: 10.1046/j.1365-2907.2003.00017.x
Young, J. K., Olson, K. A., Reading, R. P., Amgalanbaatar, S., and Berger, J.
(2011). Is wildlife going to the dogs? Impacts of feral and free-roaming
dogs on wildlife populations. BioScience 61, 125–132. doi: 10.1525/bio.2011.
61.2.7
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.
Copyright © 2019 Mori, Menchetti, Camporesi, Cavigioli, Tabarelli de Fatis and
Girardello. This is an open-access article distributed under the terms of the Creative
Commons Attribution License (CC BY). The use, distribution or reproduction in
other forums is permitted, provided the original author(s) and the copyright owner(s)
are credited and that the original publication in this journal is cited, in accordance
with accepted academic practice. No use, distribution or reproduction is permitted
which does not comply with these terms.
Frontiers in Ecology and Evolution | www.frontiersin.org 11 December 2019 | Volume 7 | Article 477