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Ecological Indicators
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A R T I C L E I N F O A B S T R A C T
Keywords: Body condition (i.e., the amount of the energy stored in organs and tissues) is a key parameter that has been
Biometrical measurements related with health, reproductive performance and density of wild ungulates including the wild boar (Sus scrofa).
Boosted regression trees In this wild pig, a reference method to assess body condition has not yet been agreed and different procedures
Brisket fat thickness have been used in recent literature. The aim of this work was to generate an easy and reliable method based on
Sus scrofa
biometrical measurements and with the ability to predict body fat in live or die boars. For this, a total of 207
hunted wild boar from three Spanish populations with contrasting food availability were included in this study.
Sex, age, biometrical parameters (body weight, total length and chest girth) and body condition indicators
(brisket and rump fat thickness, kidney fat index (KFI), ratio between chest girth-total length and scaled mass
index) were assessed for each animal. A boosted regression trees (BRT) approach was carried out to find models
based on age, sex and biometrical features that predicted brisket fat thickness in the studied animals. BRT models
including sex, body weight, total length and chest girth as explanatory variables were able to predict brisket fat
thickness in wild boar (68–73% of deviance explained). These models were not influenced by the location of
sampling and their predictive values showed a good agreement with real brisket fat thickness (94.1–95.6).
Predictive values obtained in BRT models from each area also agreed with food availability suggesting this is a
valid indicator of body condition of wild boar in a broad range of environmental conditions.
1. Introduction capacity to adapt their sizes in response to food intake. Extreme var-
iations in adipose tissue mass are commonly observed between under
Mammals require energy to support the costs of basal metabolism and overfeed individuals (Birsoy et al., 2013). Therefore, fat weight has
and other biological activities including growth, reproduction and been used for more than half a century to describe energetic status,
homeostasis. This energy is primarily stored in the form of glycogen and commonly known as body condition, in a broad number of animal
fat by several tissues and organs that in turn increase in weight when a species (Stevenson and Woods, 2006).
positive energetic balance occurs (Parker et al., 2009). Fat is a rich Body condition is a measure of the energy reserves of an organism
source of energy yielding twice as many calories than sugar or proteins linking individual fitness and the environment (Bradford et al., 2012).
and represents the main energy source of vertebrates (Drewnowski In wild ungulates, it has been related with nutritional status, health,
1992). The largest adipose tissue depots in mammals are the sub- reproductive performance and population density (Albon et al., 1986,
cutaneous white adipose tissue and the visceral white adipose tissue Brunborg et al., 2004, Bender et al., 2008, Couturier et al., 2009, Santos
(Driskell et al., 2014). These adipose tissues have an outstanding et al., 2013, Risco et al., 2016). Thus, monitoring body condition is an
⁎
Corresponding author at: Innovación en Gestión y Conservación de Ungulados SL. C/San Pedro de Alcántara 14, Cp:1001Cáceres, Spain.
⁎⁎
Corresponding author.
E-mail addresses: pgoncalvesblanco@gmail.com (P. Gonçalves), emmanuel.serrano.ferron@gmail.com (E. Serrano).
https://doi.org/10.1016/j.ecolind.2017.12.048
Received 24 October 2016; Received in revised form 5 October 2017; Accepted 18 December 2017
1470-160X/ © 2018 Elsevier Ltd. All rights reserved.
D. Risco et al. Ecological Indicators 88 (2018) 43–50
essential tool in wildlife management to assess the population perfor- 25′ 28" N, 2° 6′ 32" E) is a massif that rises over the Barcelona
mance, and eventually, to be able to detect possible imbalances before Metropolitan Area. This is an 8000 ha protected area where forest
serious problems arise (Morellet et al., 2007, Mattiello et al., 2009). formed by aleppo pines (Pinus halepensis) and holm oaks (Quercus ilex)
Different methods based on the estimation of body fat reserves have predominates. This park has a Mediterranean climate with mean tem-
been developed to measure the body condition in wild ungulates. Most peratures about 15 °C without high variation among seasons. Food
of them are invasive methods and only measurable in dead animals, like availability at CNP is moderate once, apart from natural food resources
the kidney fat index (KFI) (Riney 1955) or the bone marrow fat (Fuller (e.g. acorns) (Cahill et al., 2012), wild boar can find a great amount of
et al., 1986). Conversely, body condition in wildlife species could be domestic rubbish in bins and many times, they are artificially fed by
also measured by means of condition indices (CIs) that aim to sum- some people (Navarro-González et al., 2013a).
marize in a single value the amount of energy reserves for a given The private hunting estate (HE) is located in Oropesa (Toledo,
structural component of the body. Wildlife ecologist have developed a central Spain) (40° 00′ 41.2"N, 5° 09′ 14.3"W). This area has a con-
plethora of CIs based on relating body mass to linear measures of body tinental thermal Mediterranean climate, with hot dry summers (26 °C to
size to assess body condition in fishes (Blackwell et al., 2000), frogs, 28 °C) and mild and moderately wet winters (7 °C to 10 °C). The vege-
reptiles, birds (Green, 2001), and mammals including wild ungulates tation consists mainly of scrubland (genus Cistus), arbutus (Arbutus
(Schulte-Hostedde et al., 2001, Serrano et al., 2008). Though these non- unedo), and evergreen oak forests (Quercus suber). The area of this estate
invasive methods are very useful to assess body condition in protected (about 2000 ha) is surrounded by a fence to prevent dispersion of the
species, CIs based on biometrical measures are difficult to interpret approximately 350 wild boar that inhabit in there. Food availability is
because of the lack of studies on the relationships between these CIs and very high in this area since animals are continuously fed with a wild
direct measures of body fat reserves (Green, 2001). boar fodder (Jabalí Familia, INALSA S.A.) that is supplied in six troughs
Regarding wild suids, Stribling and Brisbin (1984) determined that located throughout the estate.
in feral swine total body fat reserves are highly correlated with brisket
fat thickness, but not with other measures and CIs such as KFI, rump fat 2.2. Wild boar sample
thickness or body mass. Therefore, methods based on brisket fat mea-
surement could be considered interesting to estimate body condition in A total of 207 wild boar were included in this study: 62 from CNP,
closely related animals such as the wild boar (Sus scrofa). Despite this, 82 from PTB and 63 from HE. These animals were hunted between
heterogeneous methods like chest girth-total length ratio (Díez-Delgado 2009 and 2011 (animals from CNP and PTB) and 2013 (animals from
et al., 2014), chest girth-total length residuals (García-Jiménez et al., HE) in different hunting events. Sampled animals from CNP and PTB
2015), KFI (Orłowska et al., 2013) or rump fat thickness (Cánovas et al., did not show significant differences in their body condition among
2015) have been used in the latest works in which body condition in hunting seasons (2009–2011), assuming similar food productivity each
wild boar has been used as a variable. year. Animals from HE are continuously fed and not differences in body
The main aim of the present work was to generate a non-invasive, condition are expected among different seasons.
easy and reliable method, based on morphometric measurements, able Sex (124 females and 83 males) and age (ranging between one
to predict the wild boar brisket fat thickness to be used as a body month to 6.5 years) of all the animals were recorded. Age was de-
condition index. Furthermore, two sub-objectives were established: 1) termined following standard methods (Boitani and Mattei, 1992,
to assess the relationships between brisket fat thickness and some body Gonçalves et al., 2016). This parameter was used to categorize animals
condition indicators of wild boar (Fat rump depth, KFI, chest girth-total in three groups: youngs (younger than 1 year), yearlings (animals with
length ratio, chest girth-total length residuals and scaled mass index ages between one and two years) and adults (older than two years). In
(SMI); 2) to explore whether these body condition indices are asso- addition, all the animals were weighted (Bw hereafter) before being
ciated with potential food availability eviscerated (+/− 1 g) and measured with a nylon tape with a nearest
precision of 0.1 cm: total length (TI. from the tip of the snout to the root
2. Material and methods of the tail) and chest girth (Chg).
This study included wild boar from two areas in Catalonia, north- 2.3.1. Brisket fat thickness and rump fat thickness
east Spain (Els Ports de Tortosa i Beseit National Game Reserve and Brisket fat thickness and rump fat thickness were determined fol-
Serra de Collserola Natural Park), and a private hunted estate located in lowing previously described procedures (Stribling and Brisbin 1984).
central Spain (Oropesa, Toledo). These study areas were selected as Briefly, we sliced through the skin and subcutaneous fat 1–2 cm to the
they represent a gradient of food availability as described below. left of the midline of the sternum, at a point about midway between the
Els Ports de Tortosa i Beseit National Game Reserve (PTB), in forelegs, and measured the brisket fat thickness with a metallic ruler to
Tarrragona province (40° 48′ 28"N, 0° 19′ 17"E) is a calcareous moun- the nearest 1 mm. Similarly we also measured the rump fat thickness by
tain region (about 35000 ha) with high orographic complexity that slicing perpendicularly through the skin and subcutaneous fat, 2–3 cm
results in a rugged and abrupt terrain with numerous ravines and steep to the left of the spine at a point about midway between the base of the
slopes. The predominant habitat in this reserve is natural pine (Pinus tail and the last thoracic vertebra (see Supplementary file 1). Rump fat
spp) grove (39%) followed by natural oak (Quercus spp) grove (15%) thickness could not be measured in animals from HE because of carcass
and its climatology is widely variable depending on the altitude with a were marketed and slicing through the skin in that area was not al-
mean temperature of 9 °C but whose range is between −9 °C in winter lowed.
and 31 °C in summer. In this area, food availability is scarce due to wild
boar sharing the limited natural resources (pastures, acorns) with do- 2.3.2. Kidney fat index (KFI)
mestic animals (mainly cattle) and no supplementary feeding is sup- KFI was assessed according to protocols previously described in wild
ported (Navarro-González et al., 2013b). boar (Orłowska et al., 2013). Kidneys together with their surrounding
Serra de Collserola Natural Park (CNP), in Barcelona province (41° fat were removed and stored in plastic bags. Once in laboratory,
44
D. Risco et al. Ecological Indicators 88 (2018) 43–50
kidneys were dried with paper towels and weighed (kidney mass, KM) Table 1
to the nearest 0.01 g without their capsule and attached fat. The at- Information about technical parameters (learning rate (lr) and tree complexity (tc)),
number of trees (Trees), percentage of deviance explained (% Dev) and relative im-
tached fat was also weighed (kidney fat, KF) and the KFI was calculated
portance (% RI) of the variables used in boosted regression tree models predicting brisket
as KF/KM (%). This parameter could not be estimated in animals from fat thickness in wild boar. Results are presented for the sum of the three studied areas and
HE and hence, it was calculated in 154 out of 207 animals studied. per area (Ports de Tortosa i Beceit National Game Reserve (PTB) and Collserola Natural
Park (CNP) from northeast Spain and private hunting states (HE) from central Spain). Bw:
2.3.3. Body condition indices based on body measurements body weight with viscera, Chg: Chest girth, Tl: total length.
Several body condition indices were calculated based on body Proposed variables Parameters Trees % Dev % RI
measurements. A ratio between chest girth and total length (Ghg-Ti
ratio), and residuals from an ordinary regression between chest girth Animals from three studied areas
and total length (Chg-Ti residuals) were calculated. Furthermore, we Bw + Chg + Tl + Sex + Age* Lr = 0.005 1050 0.73 Bw = 46.5
Tc = 2 Chg = 29.7
estimated the scaled mass index (SMI) of each animal. Scaled mass
Tl = 12.4
index is a method to estimate body condition based on the regression Sex = 11.3
between body mass and a body linear measure (total length in this case)
Bw + Chg + Sex Lr = 0.005 750 0.70 Bw = 55.2
with a statistical modifications based on central principle of scaling to Tc = 2 Chg = 32.5
solve conceptual problems generated by residual approaches (Peig and Sex = 12.3
Green, 2009). Bw + Tl + Sex Lr = 0.005 1100 0.72 Bw = 71.3
Tc = 2 Tl = 14.9
2.4. Statistical analysis Sex = 13.08
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D. Risco et al. Ecological Indicators 88 (2018) 43–50
46
D. Risco et al. Ecological Indicators 88 (2018) 43–50
condition indicator in the wild boar as summarised in Fig. 4. Further- based on such models (see Supplementary file 2).
more, BRT modelling has enabled us to generate electronic resources Explanatory variables proposed (Bw, Tl, Chg, sex and age) to predict
for wild boar managers who can introduce their own data (sex, chest brisket fat are easily measurable in both dead and live animals. Thus, to
girth, total length, body weight) and obtain a brisket fat estimation explore nutritional status of wild boar populations, we can obtain these
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D. Risco et al. Ecological Indicators 88 (2018) 43–50
Fig. 2. Partial Dependence Plots (PDP) showing the marginal effect of each explanatory variable on the response variable (brisket fat thickness), considering the average effect of the
other independent variables. PDP were obtained in models using all the studied animals, and also using exclusively animals from each of the three studied areas.
parameters in hunting events in which a representative percentage of (Massei et al., 2015) and this species has become one of the most im-
the population is hunted, or in farms where weighting and measuring portant game species in many countries, including in Spain. Many wild
wild boar is feasible. Furthermore, proposed models that do not include boar populations live in fenced estates and are fed with supplemental
all the explanatory variables have also shown a good agreement with food routinely. In this scenario, managers need validated tools to assess
real brisket fat thickness. In fact, information about sex, Tl and Chg the nutritional status of these animals in order to avoid the deleterious
could be enough to work out accurate predictions on brisket fat in the consequences of overabundance. On the other hand, studies focused on
wild boar. These measurements could be estimated using wild boar monitoring free-ranging wild boar using GPS trackers (Zoetis, 2009;
photographs taken in long distance or by camera traps, as has been Müller et al., 2013) need to assess body condition of marked animals
described in other mammals (Lambert et al., 2012; Willisch et al., before relies. We hope that this work will help researchers to easily
2013). assess body condition in live boars not only in previously mentioned
Assessing body condition using easy-measurable methods in the situations but also in further scenarios where the body condition as-
wild boar could bring important management implications. In recent sessment by no-invasive methods would be required.
decades wild boar populations have increased notably around the world
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D. Risco et al. Ecological Indicators 88 (2018) 43–50
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