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Acta Theriol

DOI 10.1007/s13364-012-0122-9

ORIGINAL PAPER

Monitoring small and arboreal mammals by camera traps:


effectiveness and applications
Anna Rita Di Cerbo & Carlo M. Biancardi

Received: 20 September 2012 / Accepted: 21 November 2012


# Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2012

Abstract Camera trapping has been widely applied to studies provides a simple non-invasive technique for collecting a large
of medium to large terrestrial mammals, but its application to amount of data per device with limited human effort.
small arboreal mammals has hardly been tested. We employed
camera trapping and other conventional monitoring methods Keywords Camera trapping . Arboreal mammals . Sciurus
during a mammal survey in a Site of Community Importance vulgaris . Sciurus carolinensis . Alien species . Survey
located within the Adda North Regional Park (Lombardy, methods
Italy). Camera trapping was particularly successful for moni-
toring arboreal mammals, allowing the first detection of pres-
ence of the invasive grey squirrel (Sciurus carolinensis) in an
Introduction
area occupied by indigenous red squirrels (Sciurus vulgaris)
and the collection of a large amount of data on squirrels and
Camera trapping (CT) has been generally used to survey
common dormice (Muscardinus avellanarius). When trig-
large- or medium-sized mammals (Datta et al. 2008;
gered, cameras were set to record short video clips (10 to
Kawanishi and Sunquist 2004; Linkie and Ridout 2011),
40 s). More than 400 events were recorded and analysed,
but rarely arboreal species (Oliveira-Santos et al. 2008;
mainly from the autumn and winter months. The daily activity
Schipper 2007), small mammals (Paull et al. 2011) or other
pattern of both species displayed a trend from two to three
vertebrates (O’Brien et al. 2010; Seki 2010; Stein et al.
activity peaks in summer to a unimodal pattern in winter, with
2008). The advantages and the limits of this technique in
the peaks of the two species temporally separated. Camera
faunistic and ecological studies have been widely debated
trapping could be a useful method also when applied to mon-
(Guil et al. 2010; Rovero et al. 2010). Nevertheless, the
itoring small mammals, particularly endangered arboreal or
potential application of camera trapping in the fields of
invasive alien species. For instance, the monitoring of the
animal ecology and conservation, including monitoring of
spread of S. carolinensis is particularly important, where the
alien species, has not been completely investigated, partic-
early detection of new population can be crucial for the con-
ularly on small and arboreal mammals (Can et al. 2011;
servation of indigenous European species. Camera trapping
Garrote et al. 2011; Munari et al. 2011; Nichols et al.
can be an effective addition to traditional survey methods. It
2011; Treves et al. 2010; Wang and Macdonald 2009).
We believe this technique is very flexible and applicable
Communicated by: Karol Zub
to arboreal as well as terrestrial animals. Therefore, we
Electronic supplementary material The online version of this article experimented the possible use of camera trapping in surveys
(doi:10.1007/s13364-012-0122-9) contains supplementary material, of small and arboreal mammals and tested its efficiency in
which is available to authorized users.
comparison with more conventional survey techniques.
A. R. Di Cerbo : C. M. Biancardi (*) Moreover, we performed a pilot study on camera trapping,
Centro Studi Faunistica dei Vertebrati, Società Italiana di Scienze
focussing on the ecology of squirrels, Sciurus vulgaris and
Naturali, Museo di Storia Naturale, C.so Venezia 55,
20121, Milan, Italy Sciurus carolinensis.
e-mail: carlo.biancardi@gmail.com The indigenous red squirrel (S. vulgaris) is declining in
A. R. Di Cerbo parts of Europe and particularly in the UK and Italy owing
e-mail: annarita.dicerbo@gmail.com to colonisation by the invasive grey squirrel (S. carolinensis),
Acta Theriol

which is native to North America and was introduced in (two cameras) and from July 2010 to March 2011 (three
Italy in 1948 (Bertolino et al. 2008; Gurnell et al. 2004b; cameras). The units were periodically moved among nine
Martinoli et al. 2010; Tattoni et al. 2006). Efficient monitoring georeferenced sites, in order to cover all sectors of the area.
methodologies for these species in critical areas are of partic- They were set to record video clips 10 to 40 s long for 24 h per
ular importance for conservation (Bertolino et al. 2009; day. At each trapping site, the camera was attached to tree
Gurnell et al. 2011). trunks at variable heights (from 30 to 180 cm). The camera
The aims of this study were (1) testing the effectiveness of objective was directed to an open area or animal trail (three
camera traps in monitoring small and arboreal mammals, (2) sites), to the understorey (four sites) or to a horizontal tree
comparing camera trapping to other census techniques and (3) branch (two sites). Sites were baited with different kinds of
discussing the results of the pilot research and their implica- food. Branches in particular were baited with hazel nuts and
tions for species management and conservation purposes. fruits (Online Resource 1). A total of 1,074 video clips were
recorded in 524 camera trap days. In the same periods, ten hair
tubes (HT) were placed in the study area. Hair tubes were
Materials and methods baited with hazel nuts and checked for squirrel hairs every
15 days (Gurnell et al. 2004a). Further, as part of a wider
The study was carried out in the Oasi Le Foppe di Trezzo mammal survey, the following methodologies were employed:
(SCI IT2050011) located in the high Po Plain (long. 9.29.57 live-trapping sessions using Sherman-like devices, collection
E, Lat. 45.37.4 N, E/W Greenwich), inside the territory of and analysis of scats of red fox and pellets of tawny owl and
the Adda North Regional Park (Lombardy, Italy). The SCI line transects for detection of individual mammals, signs,
has an area of 9.67 ha, comprising wetlands (nine artificial tracks, holes and nests, along the path around the perimeter
water basins) and lowland forest with habitats of community of the study area (Gurnell et al. 2009; Wilson et al. 1996).
interest (NATURA 2000 habitat codes 9160 and 91E0* We used the camera traps as a survey technique for
according to Annex 1, 92/43/EEC), surrounded by an agri- both terrestrial and arboreal mammals, while the other
cultural and urbanised landscape. conventional methods were applied to their specific target
Infrared camera units (Model ScoutGuard SG560) were groups. Therefore, results have been compared accordingly.
operated during two periods; from January to March 2010 The collected movies were played and carefully analysed.

Table 1 List of detected mammals

Habitus Order Common name Species CT (N) First detection Other

Arboreal Rodentia Red squirrel Sciurus vulgaris 311 CT DD, HT, SP


Rodentia Grey squirrel Sciurus carolinensis 104 CT DD
Rodentia Common dormouse Muscardinus avellanarius 7 DD CT, SP
Terrestrial Rodentia Water vole Arvicola amphibius – SP –
Rodentia Brown rat Rattus norvegicus 1 LT CT, SA, DD
Rodentia Wood mouse Apodemus sylvaticus 5 LT CT, SA
Rodentia Coypu Myocastor coypus – DD LT, SP
Erinaceomorpha Western hedgehog Erinaceus europaeus 15 CT SP
Soricomorpha Bicoloured white-toothed shrew Crocidura leucodon – LT SA
Soricomorpha Common mole Talpa europaea – SP –
Lagomorpha Brown hare Lepus europaeus 2 SP CT, DD
Lagomorpha Rabbit Oryctolagus cuniculus 8 CT DD, SP
Lagomorpha Eastern cottontail rabbit Sylvilagus floridanus 15 CT DD, SP
Carnivora Red fox Vulpes vulpes 14 SP CT
Carnivora Weasel Mustela nivalis – SP DD
Carnivora Stone marten Martes foina 7 CT SP
Carnivora Badger Meles meles 13 CT SP

CT (N) number of events recorded by camera traps, First detection the technique through which we have the first detection of each species, Other
other techniques through which we have obtained further confirmation of the species, CT camera trapping, DD direct detection by visual encounter,
HT hair tubes, LT live trapping (applied only on soricomorphs and small terrestrial rodents), SA scats or pellets analysis, SP signs of presence (scats,
tracks, nests, feeding rests)
CT was italicized to emphasize the method presented and discussed in the article from the others
Acta Theriol

Date, time, species observed, where (on a tree branch, on Therefore, we decided to consider all the recorded movies
the ground) and kind of activity were recorded into a as separate events in our pilot ecological study on squirrels.
database for further analysis. Hairs were analysed accord- The seasonal daily activity pattern of red squirrels was
ing to Teerink (1991) and individuals and other remains slightly more complex than that commonly described
and signs were identified using specific manuals (e.g. (unimodal during the cold season, bimodal from spring to
Marchesi et al. 2008). Trap days, an index of the trap- autumn, with an activity break during the hottest hours,
ping effort, were calculated as the number of devices especially in summer; Gurnell 1987). In fact, we found a
multiplied by the number of operational days (Wilson trimodal pattern during summer, with two peaks in the
et al. 1996). morning and in the late afternoon, but a third peak around
midday. In autumn, the pattern became bimodal, with two
peaks at midday and late afternoon, and unimodal in winter
Results (Fig. 1). Grey squirrels were recorded mainly during win-
ter, when their daily unimodal activity pattern did not
The identified mammal species detected during the survey, overlap with that of the indigenous species (Fig. 1,
with the methodologies employed for their detection, are Online Resource 2). These differences could provide better
listed in Table 1. Out of the 17 species recorded during the understanding of the relationship between the two squirrel
study period, 12 were detected by camera traps including all species. During our study, the indigenous and alien
three arboreal species S. vulgaris, S. carolinensis and squirrels have never been recorded together, while interac-
Muscardinus avellanarius. tions of both species with birds, in competition for food,
Therefore, CT survey effectiveness was 70.6 % overall, were observed (Online Resource 3).
both providing for the first detection of a species (41.3 %)
and a direct confirmation of its presence (35.3 %). However,
the effectiveness of CT compared to live trapping on small
terrestrial target species was 50 vs 75 %. In less than one-
third of cases, camera traps failed to capture any mammals
(29.5 %), while the average capture efficiency was roughly
1.4 animals per trap day.
The common dormouse, M. avellanarius, was first
detected in the study area by periodical artificial bird nest
surveys and was detected by camera trapping during its
nocturnal activity with a frequency of occurrence of 1.7 %,
whereas the presence of arboreal squirrels, which had been
never detected in the protected area before, was firstly
recorded by CT.
In total, the CT events involving squirrels amounted to
54.8 %, while HT gave an average result of 40 % of positive
checks (red squirrel only). Records of red and grey squirrel
were in the approximate ratio of 3:1 (Table 1).
No grey squirrel hairs were found in HT, while the
species was first recorded in a video clip. After the first
encounter, more CT events and some direct observations of
squirrels were recorded.
The choice of the intermission length (time interval
between two captures) basically depends on the purpose of
the study and ranged from 0 to 30 min (Koerth and Kroll
2000; O’Brien et al. 2003; Otani 2001). When set to record
short movies, camera traps could be useful to study the active
period, the behaviour and the activity budget of a species.
Squirrels are capable of rapid and frantic movements, and we
noticed that in most cases, two subsequent captures of the
same animal could be related to different events. For exam-
ple, the collection of different food items and the search for
food in different places after moving a short distance. Fig. 1 Seasonal daily activity pattern of red and grey squirrels
Acta Theriol

Discussion Our survey and ecological observations are important for


the survival of the local red squirrel population, allowing the
Generally, conventional methods for animal surveys have management of the protected area to plan rapid actions in
both advantages and disadvantages: they allow species favour of the indigenous species. In fact, the early detection
identification (i.e. live trapping, hair collection) and abun- of alien grey squirrels in new patches can be crucial in the
dance estimation (i.e. capture–recapture), but all of them battle for red squirrel conservation (Martinoli et al. 2010).
require high human effort and some may have a direct In conclusion, we found camera trapping to be an effec-
impact on the animals (i.e. direct disturbance or affect their tive technique for recording arboreal and low-population-
behaviour). density small mammal species, and we recommend its use in
For instance, live trapping of small mammals might lead conjunction with traditional methodologies. The effective-
to major physiological disturbances (e.g. hypothermia, hy- ness of monitoring the spread of invasive and problematic
perthermia, stress, shock) owing to temporary restraint and species, such as the alien grey squirrel, could be greatly
handling and generally requires a great effort, with an effi- improved by the use of camera traps.
ciency that seldom exceeds 15–20 % (Torre et al. 2010).
Less effort and good results can be obtained using HT for
Acknowledgments Fieldwork was funded by Adda North Regional
surveys of arboreal species, with efficiencies above 50 % Park for the Management Plan of SCI IT2050011. Partial results have
(Suckling 1978). According to Mortelliti and Boitani been presented as poster to the Problematic Wildlife II International
(2008), the most efficient and cost-effective technique used Congress, Genazzano, Italy, February 2011. We are grateful to Dr.
Sergio Saladini (Director) and Dr. Giuliana Defilippis (Resp. for Nat-
to assess the presence/absence of arboreal squirrels is sur-
ural Resources) of the Adda North Regional Park and Fabio Cologni
veying with hair tubes. However, considering the possibili- and all the WWF volunteers of the Oasi Le Foppe of Trezzo sull’Adda
ties of identification errors between related species owing to (MI). We also wish to thank two anonymous reviewers for their most
similar cuticular patterns and medullary structure (Teerink valuable suggestions and advice.
1991) and considering the time and cost of hair analyses, CT
could be extremely effective, both in term of cost and
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