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ORIGINAL PAPER
Wildl. Biol. Pract., 2011 December 7(2): 1-14
doi:10.2461/wbp.2011.7.11
Copyright © 2011 J. Bernardino, R. Bispo, P. Torres, R. Rebelo, M. Mascarenhas & H. Costa.
This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distri-
bution, and reproduction in any medium, provided the original work is properly cited. Published by: Portuguese Wildlife Society.
En h a n c i n g ca r c a s s rE m o v a l Tr i a l s a T Th r E E Wi n d En E r g y Fa c i l i T i E s i n
Po r T u g a l
J. Bernardino1,*, R. Bispo2, P. Torres1, R. Rebelo3, M. Mascarenhas1 & H. Costa1
1 Bio3 Estudos e Projectos em Biologia e Valorização de Recursos Naturais, Lda., Rua D. Francisco
Xavier de Noronha, 37B 2800-092 Almada, Portugal.
2 Grupo de Estatística e Matemática, Instituto Superior de Psicologia Aplicada, Rua Jardim do tabaco, 34,
1149-041 Lisboa, Portugal.
3 Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, Avenida Nª
Senhora do Cabo, Nº 939, 2750-374 Cascais, Portugal.
* Corresponding author: e-mail: joana.bernardino@bio3.pt; Phone: +351 212-951-588
Keywords
Bird Mortality;
Carcass Removal Trials;
Monitoring;
Survey Effort;
Survival Analysis;
Wind Farm.
Abstract
During the last years there has been a signicant worldwide increase in
the number of wind farms. This kind of energy can have negative impacts,
such as the direct mortality or lethal injury of birds and bats caused by
collision with wind turbines. In order to evaluate bird (or bat) mortality
regarding wind power generation facilities, strict monitoring protocols are
required which must take into account the possibility of carcass removal
by scavenging animals or decomposition before the monitoring session.
For this purpose, carcass removal trials with 180 carcasses representing
three size classes (small, medium and large) were conducted in two seasons
(Spring and Autumn) at three wind farms located in the central region of
Portugal. No signicant differences were found between removal rates of
different wind farms or size classes contrarily to seasons, which presented
an average carcass removal time of 3.9 and 4.6 days, respectively for Spring
and Autumn. The results of the present study showed the importance of trials
to estimate the carcass removal rates, which inuences the survey effort
management and consequently the monitoring protocols. The experimental
design for future trials in the same region should account for season effect
and be conducted using daily checks of the carcasses for, at least, 15 days.
Introduction
Nowadays, wind is considered worldwide as one of the most promising energy
sources found in nature. Despite the obvious benets of wind turbines as a clean
energy source, the construction of wind farms can be responsible of impacts on
ying vertebrates, such as fatality through collision with rotating turbine rotor
blades, habitat modication, barrier effect or disturbance in nesting areas [1-4].
These impacts, especially the birds and bats mortality, became a source of major
concern among a number of stakeholder groups [5-10]. In fact, results obtained
during several monitoring studies indicated that wind farms were responsible for the
2 || J. Bernardino et al. | Enhancing Carcass Removal Trials at Three Wind Energy Facilities in Portugal
decrease in some species’ populations [11-14] although many other studies revealed
that these impacts were not important when compared to those originated by other
infrastructures [15-17]. Nevertheless, the potential for wind farms to affect bird or bat
populations should not be underestimated [11,18].
During the last two decades, the need to properly assess the impacts on ying
vertebrates led to the development of methodologies for evaluating bird and bat
fatalities in existing and planned wind facilities developments. Current post-
construction monitoring protocols require that carcass estimates under turbines are
adjusted taking into consideration the rate at which carcasses decompose or are
removed by scavengers [2,19,20]. Therefore, most recent studies include carcass
removal trials, although few follow the exact same protocols [21,22]. Furthermore,
even fewer studies have been conducted with the specic aim of improving the
protocol design for this kind of trials [23,24]. Thus, it is necessary to develop a single
and robust methodology in order to validate any results or comparisons between wind
farms, allowing at the same time a correct evaluation of the impacts regarding its
construction [17].
Over the years protocols have tended to become more strict and demanding
[19,20,25-27]. However, they often increase the monitoring costs, which is a problem
due to the limited budgets of many monitoring studies. Hence, it is crucial to develop
efcient methodologies that consider cost/benet relationships [28], maximizing
effort reduction without compromising the quality of the results. To achieve this
goal, it is necessary to clarify the inuence of effort reduction in monitoring and
consequently in a correct assessment of the results.
The aim of this study was to evaluate the importance of conducting carcass removal
trials in order to achieve a correct evaluation of bird mortality regarding wind power
generation facilities, and to optimize the survey effort employed in monitoring
protocols. It was conducted with data collected during monitoring studies of bird
mortality at three Portuguese wind farms.
Methods
Study area
The studied wind farms are located at the central region of Portugal (Fig. 1), each
comprising a series of mountain ridges.
Caramulo wind farm is situated at Serra do Caramulo (maximum altitude of
1076.57 m a.s.l.) and comprises 45 wind turbines subdivided along ve smaller units,
each turbine with a power of 2.0 MW. The vegetation consists mainly in shrubs and
scattered trees (Quercus robur and Quercus pyrenaica) on the mountain ridges, and
cereal elds in some areas. Average annual temperature and rainfall vary between 10-
12.5ºC and 2000-2400 mm, respectively. This facility is supported by Generg Ventos
do Caramulo, Lda. (Portuguese Promoter GENERG Group).
Pinhal Interior wind farm also comprises several smaller units along Serra de Alvelos
(1084 m), Cabeço da Rainha (1080 m), Moradal (885 m) and Perdigão (566 m), consisting
in 58 wind turbines, each with a power of 2 MW, with the exception of Alvelos, which
Wi l d l i f e Bi o l o g y in Pr a c t i c e 2011, 7(2) || 3
presents each turbine with a power of 3 MW. In the last decades the autochthonous
vegetation has been replaced by pine (Pinus pinaster) and eucalyptus (Eucalyptus
globulus) trees, however due to forest res most of the area is now occupied by low-
growing shrubs of the genus Erica and related genera. Average annual temperature
ranges from 7.5 to16ºC and rainfall from 800 to1600 mm. This wind farm is supported
by GENERVENTOS do Pinhal Interior – (company also included in Generg Group).
Lousã wind farm, located at Serra da Lousã (maximum altitude 1205 m a.s.l.),
comprises 14 wind turbines, each with a power of 2.5 MW. The vegetation consists
in low shrubs (Erica sp. or Calluna vulgaris), herbaceous vegetation, oak forests
and plantations of coniferous and mixed woods [29]. In this area, average annual
temperature ranges 9-22ºC and rainfall 1000-1800 mm. Parque Eólico do Trevim,
Lda (Iberwind Group) manages this facility.
Fig. 1. Location of each wind farm in Portugal. Black dots represent single wind turbines.
4 || J. Bernardino et al. | Enhancing Carcass Removal Trials at Three Wind Energy Facilities in Portugal
Field methods and analytical approach
The carcass removal trials were conducted in two seasons (Spring - May/June;
Autumn – September/October) since, according to the monitoring protocol design
for all three wind farms, carcass searches are restricted to these periods [30-32].
Specically, Spring trials were performed from the 7th until 27th of May, 14th of
May until 8th of June and from 6th until 30th of June for Lousã, Pinhal Interior and
Caramulo wind farms, respectively. During the second season (Autumn), the trials
were conducted between day 3 and 23 of October, in all sites.
Complete and fresh carcasses of parakeets (Melopsittacus undulates), quails
(Coturnix coturnix) and partridges (Alectoris rufa) were used to represent birds
of three size classes (small – ≤15 cm and ≤50g, medium – 15-25 cm and 50-200g;
large – ≥25 cm and ≥200g) and more accurately reect realistic removal rates
[33]. Carcasses were obtained in avian breeding facilities. Handling was always
performed with lab gloves to prevent human odour contamination.
In each farm, 10 carcasses of each size class were placed per season, comprising
a total of 180 corpses. The carcasses were placed near the turbines or associated
infrastructures (range 8- 42 m distance), randomly, independently of the size class,
and at a minimum distance of 500 m from each other. After its placing, all carcasses
were checked daily, every morning, until their removal for a maximum period of 20
days.
Statistical approach
Carcass removal trials involve measuring the time until carcass removal. The
obtained data were examined using Survival Analysis [34]. Standard statistical
approaches were discarded based on the positively skewed removal time distribution
[35] and on the presence of censored observations (carcasses with removal times
beyond 20 days).
The survivor function, that in this context describes the probability of a carcass
being removed beyond a time t (or persist until t), was estimated using the Kaplan-
Meier estimator. The Log-Rank test was used to test the existence of signicant
differences between survival curves of different farms, seasons and size classes
[36].
Also, according to the variety of survey effort methodologies used in the last
decade in monitoring studies, some reduction effort scenarios were selected to
evaluate its inuence in the results obtained, by comparing it to the used eld effort
methodology (daily checks through 20 days). The resulting survivor distributions
were compared using the Wilcoxon test. Four inspection scenarios were tested
against the used methodology, in all wind farms:
- Daily checks for 14 days [37];
- Daily checks for 7 days [38];
- Checks every other day for 20 days;
- Daily checks in the rst 4 days and then in the 7th, 10th, 14th and 20th days [39].
Statistical analysis was performed using R software [40]. Data were analysed
under a 0.05 level of signicance.
Wi l d l i f e Bi o l o g y in Pr a c t i c e 2011, 7(2) || 5
Results
The majority (>80%) of the 180 carcasses used was removed in the rst week after
its placement (Fig. 2). After the 15th day, none of the carcasses were removed until
the end of the sampling period, disappearing eventually by decomposition (n=13).
Fig. 2. Histogram of the removal times of non censored carcasses.
The Log-Rank test (Fig. 3) showed no signicant differences for the carcass removal
times between farms (χ2= 4.5; d.f. = 2; p = 0.107) or size classes (χ2= 1.9; d.f. = 2;
p = 0.384). However, removal times differed signicantly between seasons (χ2= 5.3;
Fig. 3. Survival functions determined with the Kaplan-Meier estimator. A - between seasons; B - between
wind farms; C - between carcass sizes.
6 || J. Bernardino et al. | Enhancing Carcass Removal Trials at Three Wind Energy Facilities in Portugal
d.f. = 1; p = 0.021). The data analysis showed that in Spring the carcasses were removed
faster, with almost 80% disappearing in the rst 5 days (Fig. 4). In Autumn, within
the same period, only 60% of carcasses were removed, reecting a lower carcass
removing probability throughout the sampling period (20 days). Mean carcass removal
time (standard deviation in brackets) in the wind farms was 3.9 (0.34) and 4.4 (0.37),
respectively in Spring and Autumn.
Considering the survey effort comparisons, once no carcasses were removed after
the 15th day, there were no changes in the survivor curves of any wind farm when
the trial length was reduced from 20 to 14 days. However, when the survey effort
was reduced to 7 days (Fig. 4A) the resulting survivor curves differ signicantly
for both seasons (p=0.0346 and p=0.0143, for Spring and Autumn, respectively).
Also, when the survey effort reduced to one check every other day (Fig. 4B) the
curves differed signicantly for both seasons (p=0.022 and p=0.014, for Spring and
Autumn respectively). Considering the last scenario, the survey effort consisted in
daily checks in the rst 4 days followed by surveys conducted only on the 7th, 10th,
14th and 20th days (Fig. 4C), again the survivor curves differed signicantly for both
seasons (p=0.005 and p=0.002, for Spring and Autumn respectively).
Fig. 4. Survival functions determined with the Kaplan-Meier estimator according to the survey effort
performed. A - comparison between daily checks for 20 and 7 days, for both seasons; B - comparison
between daily checks and every 2 days, for a period of 20 days, for both seasons; C - comparison between
daily checks and checks every day until the 4th day and then only in the 7th, 10th, 14th and 20th days, for a
period of 20 days, for both seasons.
Wi l d l i f e Bi o l o g y in Pr a c t i c e 2011, 7(2) || 7
Discussion
In our study we did not found a signicant effect of bird size on carcass removal
times. This may be related with specic biophysical characteristics of the mountain
ridges, since the same result has been observed in other regions of Portugal [41]. In
contrast, studies performed for instance in the north of Portugal, with exactly the same
species, detected signicant differences in removal rates between class sizes [42].
Nevertheless, in this study signicant differences were detected between seasons, with
the corpses disappearing faster in spring/early summer than in autumn. This result is
similar to those described in several other studies performed at Portuguese wind farms
[43-45] possibly due to different scavengers activity between seasons [22].
Although the differences between seasons seem relatively small and some times
negligible, they must be taken into account, since it can produce signicant bias
in the mortality estimates (Table 1). To exemplify the importance of even slightly
different removal rates, let’s consider that the mortality rate (number of corpses per
period of time) can be simply estimated by:
M =
where Ci, is the total number of carcass found at the i-th search; ri the removal
correction factor ( proportion of carcasses that persist unscavenged at the i-th search);
and p the detection rate (in this case, we assume 0.25)[46]. Considering that, during
one of the Spring searches, the carcass of 1 bird, which died 5 days before, is found,
the removal correction factor is 0.23, which would result in a mortality estimate of,
approximately, 17 birds (i.e. M= 1/(0.25×0.23)), for that period of time. However,
if the same situation occurred during Autumn, the mortality estimate would be
considerably lower, 10 birds (i.e. M=1/(0.25×0.40)). Naturally, the estimates differ
even more as the number of observed mortality and the time between the bird´s death
and the i-th search increases (e.g. C=5, found 7 days after death; M=143 and M=91,
respectively, during Spring and Autumn).
Table 1. Mortality estimate (estimated by estimator presented in [46]), considering different removal rates
(r) and a detection rate (p) of 0.25. C- Number of carcass found at the i-th search.
Days since
death
Spring Autunm
Removal
rate (r)
Mortality estimate (M) Removal
rate (r)
Mortality estimate (M)
C=1 C=2 C=5 C=1 C=2 C=5
1 0.81 4.9 9.9 24.7 0.84 4.8 9.5 23.8
2 0.63 6.3 12.7 31.7 0.67 6.0 11.9 29.9
3 0.40 10.0 20.0 50.0 0.56 7.1 14.3 35.7
4 0.29 13.8 27.6 69.0 0.48 8.3 16.7 41.7
5 0.23 17.4 34.8 87.0 0.40 10.0 20.0 50.0
6 0.19 21.1 42.1 105.3 0.31 12.9 25.8 64.5
7 0.14 28.6 57.1 142.9 0.22 18.2 36.4 90.9
Despite the differences between seasons, the high rate at which the carcasses were
removed in the three wind farms was similar to that reported for other studies developed
at North America and Europe, in similar mountain ridges [9,47-51], with more than 80%
8 || J. Bernardino et al. | Enhancing Carcass Removal Trials at Three Wind Energy Facilities in Portugal
of the carcasses removed until the end of the rst week. Strickland et al. [52] reported
the mean carcass removal time between six and seven days for birds and about 10 days
for bats at Buffalo Ridge, Minnesota. Also at this site, Higgins, Dieter, and Usgaard
[9] reported scavenging of 12 from 15 carcasses (80%) after one week (two trials). At
Vansycle wind farm located primarily in wheat elds, small carcasses lasted on average
15 days [39]. At the Buffalo Ridge Wind farm, small carcasses persisted on average 4.7
days, whereas small birds at Foote Creek Rim persisted 12.2 days [48]. Also, Wobeser
& Wobeser [53] reported that nearly 80% (79.2) of the chicks placed in a mixed grazed
pasture were removed within 24 hours. In France, Pain [54] estimated duck carcasses
lasted an average of 1.5 days in open vegetations, whereas those concealed by vegetation
or those in water lasted 3.3–7.6 days. At Tehachapi Pass (EUA) small and large carcasses
endured an average of 3.1 and 2.12 days, respectively [48].
This high decrease of animal corpses in the rst days clearly inuences the survey
effort management and monitoring protocols, mainly regarding the estimation of
removal/decomposition rates and consequently the mortality evaluation in wind farms.
No signicant differences were found in the survivor curves when the trial length was
reduced from 20 to 14 days, which is explained by the absence of carcass removal in
this last ve days. In the scenarios where the survey effort was considerably reduced, the
resulting survivor curves changed signicantly. For example, during Autumn with daily
checks, the carcass persistence probability at the end of 6 days was 30%, while in the
last scenario tested (daily checks in the rst 4 days and then in the 7th, 10th, 14th and 20th
days) this probability increased to 50%, underestimating the wind farm mortality rate.
Therefore, in similar mountain ridges it seems advisable to check carcasses daily, for a
minimum period of time of 15 days.
Although these results cannot be directly extrapolated to others regions, considering
that the majority of studies also presented removal rates specially high during the rst
days of the trails, is legitimate to assume similar results in other wind farms, which
highlights the importance of developing strict monitoring protocols, mainly regarding
survey effort. According to Table 2, within 30 monitoring studies performed in the last
decade with removal trials, 43.3% carried out daily checks for a minimum of 14 days.
Still, the majority of these studies presented monitoring protocols less strict, justied by
nancial and logistical limitations that must be contested facing these results.
In the three wind farms studied, and since the inspection periods were restricted, the
removal trials had to be performed just in two seasons (Spring and Autumn). Thus,
further research should be conducted at several other wind farms located in the same
region, especially during winter and summer, in order to determine if the differences
between the removal times remain. In fact, recent guidelines recommend that removal
trials should be performed at least four times a year [20]. As explained above, small
differences regarding the removal rates can signicantly bias the mortality estimates.
So, if no previous studies have been conducted in the vicinity of a new wind farm,
we propose that the removal trials should be performed throughout a year (to include
seasonal effects), with daily checks. Once these rigorous trails have been conducted
(considering different seasons, carcass sizes, etc.) and similar conclusions have been
achieved for the region, the team responsible for developing the monitoring program
of a new wind farm should be able to evaluate if new removal trails are really needed
or if they can be redesign. Nevertheless, it is clear that further studies are required to
optimize the trials design and achieve the best cost/benet relation.
Wi l d l i f e Bi o l o g y in Pr a c t i c e 2011, 7(2) || 9
Acknowledgments
The authors would like to thank those who took part in the eld work. We also would like to thank Bio3
Lda, for all nancial and logistical support, and Grupo GENERG – Gestão e Projectos, SA and Iberwind
Group that allowed accomplishing this study in Caramulo, Pinhal Interior and Lousã wind facilities.
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