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Ecological Indicators 55 (2015) 5258

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Presence of Cuckoo reliably indicates high bird diversity: A case study


in a farmland area
Piotr Tryjanowski a , Federico Morelli b,
a

Institute of Zoology, Poznan University of Life Sciences, Wojska Polskiego 71C, PL-60-625 Pozna
n, Poland
Czech University of Life Sciences Prague, Faculty of Environmental Sciences, Department of Applied Geoinformatics and Spatial Planning, Kam
yck 129,
165 00 Prague 6, Czech Republic
b

a r t i c l e

i n f o

Article history:
Received 8 October 2014
Received in revised form 7 March 2015
Accepted 10 March 2015
Keywords:
Bioindicators
Cuculus canorus
Species richness hotspots
Top predators

a b s t r a c t
Here we studied the occurrence of Cuckoo Cuculus canorus and top predators as indicators of biodiversity
in agro ecosystems of Western Poland, to identify local hotspots. Bird species richness and land-use
diversity were used as measures of biodiversity. The relationship between the presence of Cuckoos and
four avian top predators with biodiversity measures were examined using Generalized Linear Mixed
Models.
Cuckoos were mainly distributed on sites with greater species richness, but were absent from the low
species richness sites, while the top predators were distributed uniformly. The performance of the best
models using the presence of Cuckoo was 27% higher than the best models using top predators. Our results
highlight the predictive capacity of Cuckoos as an indicator of bird species richness than top predators
and the usefulness of this species in biodiversity studies. The cookoo is charismatic, widespread across
the main types of landscapes, and is easy to detect from its song. Importantly, our ndings propose that
cookoo can be used as effective and cheap tool to monitor the high bird diversity in different European
countries.
2015 Elsevier Ltd. All rights reserved.

1. Introduction
One of the central themes in ecology is to understand the distribution and the abundance of species, including those that are
coevolving (Thompson, 2005). Coevolution is the process by which
species specialise in their interactions with one another, and the
way in which these specialised relationships results in reciprocal
evolutionary changes. For this reason, studies of coevolution can
be useful for understanding the causes of biodiversity distribution
in the landscape (Poulin and Morand, 2005; Thompson, 2005). The
role of biodiversity is crucial for conservation and the functioning
of ecosystems (see for example Schwartz et al., 2000). Biodiversity
can be studied by focusing on species richness and taxonomic, phylogenetic and functional diversity (Devictor et al., 2010). However,
the study of biodiversity is difcult; data can be hard to collect and
studies time consuming, and hence costly. Consequently, the use of
tools to indirectly estimate an ecosystem may prove helpful. One
way of improving the knowledge of biodiversity is to identify its
measurable attributes or surrogates (Magurran, 2004; Noss, 1990).

Corresponding author. Tel.: +393282097285.


E-mail addresses: fmorellius@gmail.com, morellius@libero.it (F. Morelli).
http://dx.doi.org/10.1016/j.ecolind.2015.03.012
1470-160X/ 2015 Elsevier Ltd. All rights reserved.

The complexity of ecosystems has led to the development and


use of surrogates to simplify, represent, and help manage complex
systems. Some have evn described the use of surrogates of biodiversity as a holy grail of conservation (Lindenmayer et al., 2014).
However, the effectiveness of surrogates is hard to determine, and
despite the considerable importance these ecological tools have
for conservation planning, they continue to produce varied and
conicting results (Grantham et al., 2010). For instance, avian top
predators have characteristics that could make them suitable as
indicators of biodiversity hotspots (Cabeza et al., 2007). The debate
about the usefulness of birds other than raptors has reignited in
the past ten years (Cabeza et al., 2007; Sergio et al., 2008, 2005).
Studies on the association between the occurrence of top predators
and biodiversity have been particularly criticized. The criticisms on
the use of raptors as charismatic birds as surrogates of biodiversity
included methodological biases introduced in the sampling design
and low effectiveness of the approach when applied to different
environments (i.e., lack of transferability) (Kry et al., 2007; Roth
and Weber, 2008).
The chief characteristics of a reliable surrogate as bioindicator
are that it must be: (1) sufciently sensitive to provide an early
warning of change; (2) widely applicable in nature; (3) capable of
providing a continuous assessment over a wide range of perturbed

P. Tryjanowski, F. Morelli / Ecological Indicators 55 (2015) 5258

environmental conditions; (4) independent of sample size; and (5)


easy and cost-effective to measure, collect, assay, and calculate.
For these reasons, we believe that the Cuckoo Cuculus canorus is
potentially a good candidate as an indicator in biodiversity studies
because is it widespread and common in European agroecosystems
(Morelli et al., 2014; Tryjanowski et al., 2011). This species is characterized by the highest rate of detectability (characteristic, with
loud vocalizations or songs, which favors surveys), it arrives late
in the breeding season and hence has the ability to be distributed
relative to the distribution and the abundance of other species that
have already started to reproduce (Tryjanowski et al., 2005), and
it has a specic relationship with many potential host populations
(Stokke et al., 2007; Wesoowski and Mokwa, 2013), which are parasited. Avian brood parasitism is a reproductive strategy by which
parasites lay their eggs in the nest of other species, the hosts, which
incubate and rear the parasitic offspring (Davies, 2011; Soler et al.,
1999).
Hence, we hypothesize that Cuckoos function as better indicators than top predators to study and predict the patterns of bird
diversity in an area. The aim of this study was to assess the predictive power of the occurrence of Cuckoos as indicators of bird species
richness, and secondly to compare the goodness of t of predictive
models using Cuckoos and the presence of avian top predators on
biodiversity estimated as total bird species richness and land use
diversity.

53

Table 1
List of bird species most used as host by cuckoo Cuculus canorus following
Wesoowski and Mokwa (2013), relative frequency of parasitation used to rank in
this study the sampled sites on the presence of potential hosts.
Specie

Frequency of host (%)

Acrocephalus scirpaceus
Lanius collurio
Acrocephalus palustrisa
Phylloscopus sibilatrix
Motacilla alba
Phoenicurus ochruros
Erithacus rubecula
Prunella modularis
Sylvia communis
Hirundo rustica
Saxicola rubetra
Acrocephalus arundinaceus
Anthus trivialis
Phoenicurus phoenicurus
Sylvia curruca
Troglodytes troglodytes
Alauda arvensis
Muscicapa striata
Turdus merula
Hippolais icterina
Phylloscopus collybita
Motacilla ava
Sylvia atricapilla
Sylvia borin
Sylvia nisoria

32.4
16.9
8.5
6.3
5.6
4.9
4.2
3.5
2.4
2.1
2.1
2.1
1.4
1.4
1.4
1.4
1.2
1.2
1.2
0.7
0.7
0.7
0.7
0.7
0.7

2. Methods
2.1. Study area
The study was conducted in the agricultural landscape of Western Poland, near Odolanw (51 34 N, 17 40 E). The study area
(141 km2 ) is an extensively used agricultural landscape that comprises a mosaic of meadows and pastures (44%), arable elds (42%),
mideld woodlots of different ages (6%), and scattered trees and
discontinuous linear habitats, mainly mixed rows of trees and
shrubs (see details in Hromada et al., 2002).
2.2. Bird data collection
We obtained data on bird species richness and abundance by
using ve-minutes point counts carried out at 59 sites each month
during the breeding season AprilJune 20092012. Every site comprised three points (each as a vertex of a triangle) at a distance of
at least 300 m from each other at which observers counted birds
from three independent directions (15-min bird count). All counts
were performed between half an hour and four hours after sunrise, but only during favorable weather conditions (i.e., no rain or
strong wind). Point counts provide highly reliable estimates of relative population density using this recognised, standardized method
to compare bird communities among habitats and temporal scales
(Bibby et al., 1992). The survey of breeding raptors in the sample
sites was performed during the same period, using point counts
and, additionally, searching for nests to conrm the presence as
breeding species. The raptor species considered in this study as
top predators were Buzzard Buteo buteo, Goshawk Accipiter gentilis,
Sparrowhawk Accipiter nisus and Kestrel Falco tinnunculus. These
species were selected because they have already been used in other
studies (Sergio et al., 2006, 2005) and because they are well distributed in the study area.
2.3. Biodiversity measures
We used two measures of biodiversity. The rst measure was
related to the biological diversity of bird species and the second to
land use diversity or landscape heterogeneity.

Bird species richness (BSR) was used as a biodiversity measure,


because it is a basic surrogate for the more complex concept of ecological diversity (Magurran, 2004; Morelli, 2013). Species richness
is the most popular diversity index in ecology and, according to
some studies, is a better surrogate of biodiversity or habitat condition than other biodiversity indices (Young et al., 2013). At each site
sampled, species richness was calculated as the sum of all recorded
bird species.
Land-uses diversity (LUD) is a surrogate of available trophic
niches and therefore of potential biodiversity (Kisel et al., 2011).
The LUD was calculated using the Shannon-Weaver diversity index,
with the formula H = pi ln(pi ), where the different pi are the proportions of the different land use types in the area surrounding
the sample site within a radius of 100 m. The typologies of landuses considered in this study were: cultivated, grassland, forest,
reforestation, riparian, hedgerows, isolated trees, shrubs, building,
roads, railways, rivers and water.
In order to study the birds that the are potential hosts of Cuckoos,
host species were counted and then birds were ranked according to the most frequently parasitized species recorded in Poland
(Wesoowski and Mokwa, 2013). The rank for the site was calculated as the summatory of values per bird species host (Table 1),
after the application of a standardization method to these values
from the vegan package in R (Oksanen, 2014).
2.4. Statistical analyses
The sampled sites were treated as statistically independent
observations because the values of spatial autocorrelation between
geographic distance and land use dissimilarity of sites was low
(Mantel test r < 0.12, n = 59 sampled sites, p > 0.05) (Manly, 2006).
Dissimilarity indices among land use composition at sampled sites
were calculated using the vegdist function of the vegan package
for R (Oksanen, 2014), applying the Srensen index of dissimilarity
between pairwise sites for land use composition.
The relationship between the two biodiversity measures (BSR
and LUD) measured in this study was quantied by means of a
Pearson correlation test.

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P. Tryjanowski, F. Morelli / Ecological Indicators 55 (2015) 5258

The nature and strength of relationships between Cuckoo occurrence, top predator occurrence and measures of biodiversity (BSR
and LUD) on sample sites were examined using Generalized Linear
Mixed Models (GLMM) (McCullagh and Nelder, 1989) by including year and sampled sites as a random factors in the models.
The occurrence of Cuckoo and top predators was used as response
variables (species occurrence), assuming a binomial distribution
and the two biodiversity measures (BSR and LUD) were used as
predictors. The GLMMs were t by maximum likelihood (Laplace
approximation).
The predictive capacities for Cuckoos and top predators used as
surrogates of biodiversity were compared using the area under the
receiver operating characteristic (ROC) curve (AUC) of the respective logistic models, calculated for all years separately. The ROC is
a graphical plot which illustrates the performance of a binary classier system as its discrimination threshold is varied. It is created
plotting the fraction of true positives out of the positives (true positive rate) vs. the fraction of false positives out of the negatives (false
positive rate) at various threshold settings. The AUC calculated for
each model indicates the predictive performance expressed as an
index ranging from 0 to 1 (DeLong et al., 1988).
A further validation was performed applying GLM to the 2009
breeding season, and using as response variable the bird species
richness, specied as a Poisson distribution, and land-uses diversity with occurrence of Cuckoo rst, and then land-uses diversity
with occurrence of top predators, as covariates. The predictions of
these models were used to study the spatial mismatch between real
pattern of bird diversity and predicted values.
The relationships between the occurrence of Cuckoos and top
predators with bird species richness were explored graphically by
means of the ArcGIS tool inverse distance weighted (IDW). The
IDW is a technique that interpolates a raster surface from several
point values (BSR or LUD) and distances among points (Lu and
Wong, 2008). Here, we compared the patterns among the values
of real bird species richness and the predicted bird species richness, obtained from the output of the modelling approach. We
performed a Mantel test on the results after they were rearranged as
a matrix of distance among pairwise sampled sites (Mantel, 1967).
This procedure was used to verify the existence of spatial patterns
(correlations) between observed values as BSR and predicted values obtained from Cuckoo and top predator models. The Mantel
test compares two similarity or distance matrices computed for
the same sites (Legendre and Legendre, 2012). The distance matrices were calculated as distances among values recorded for each
sampled site using the ade4 package. If a signicant correlation
exists, then the pattern distribution of values would be similar.
The Mantel statistic (rM ) is a measure of the correlation between
two matrices and it results from the cross-product of the matrix
elements after standardization. The Mantel statistic is bounded
between 1 and +1, and it behaves like a standard correlation coefcient. In the Mantel test we used 9999 permutations of N rows
and columns of the matrix.
Finally, the possible relationship between the density of potential preferred hosts and Cuckoo distribution was tested adding both
the richness of host species and the ranked values of each sampled
site to the predictors of the Cuckoo model. All tests were performed
with R (R Core Team, 2014).

3. Results
3.1. Biodiversity pattern and occurrence of Cuckoo and top
predators
During the four years of study we sampled 59 sites counting
a total of 157 bird species during the breeding season including

17 raptor species. The most abundant bird species were Skylark


Alauda arvensis (91.2%), Yellowhammer Emberiza citrinella (82.5%)
and Corn Bunting Milaria calandra (63.2%), and among raptors Buzzard (25.1%), Marsh harrier Circus aeruginosus (5.8%) and Kestrel
(3.3%). Abundance of the different species is provided in Electronic
Supplementary material Table ESM1.
The frequency of occurrence of Cuckoo in the sampled sites was
22%, and the frequency of top predators (Buzzard, Goshawk, Sparrowhawk and Kestrel) was 25%. Thus both frequencies were similar
and comparable in the study area.
Bird species richness (BSR) ranged from a minimum of four to a
maximum of 30 species. The average was 13.78 bird species with a
standard deviation of 4.54.
The land-uses diversity (LUD) index ranged from a minimum of
0 (homogeneous land use coverage at the sampled site) to a maximum of 1.98. The average was 1.26 with a standard deviation of
0.38. The two variables (BSR and LUD) were positively correlated
(r = 0.29, p < 0.05).
Cuckoos were mainly distributed at the sampled sites with
greater BSR in all years. This species was present only when BSR
was equal to or larger than seven species, and it was absent from
sites characterized by the lowest values of BSR. The top predators were distributed more uniformly across all the sampled sites,
independently of their values of species richness (Fig. 1). Furthermore, the spatial distribution of Cuckoos was more strongly
related to BSR than the spatial distribution of top predators. As
such, the results of Mantel test showed better congruence between
observed BSR and predicted BSR, when using Cuckoos occurrence
(rM = 0.22, p < 0.05, nrepet = 9999) than using top predators occurrence (rM = 0.11, p > 0.05, nrepet = 9999) as predictor (Fig. 2).
3.2. Model results and performance
The occurrence of the Cuckoo and top predators was signicant
positively correlated with the two measures of biodiversity. However, only BSR was signicant and so was selected as the predictor
in the model procedure (Table 2).
The performance of the best models for Cuckoos showed the
highest goodness of t and the best predictive capacity compared to
the best models using the presence of top predators as a surrogate
of biodiversity for all years (Fig. 3, AUC averaged). In analyses of
single raptor species, the only signicant species were Buzzard and
Kestrel, both showing performances inferior to the performance of
top predators (AUC < 0.59).
The density of potential preferred hosts (richness of host or
ranked values of each sampled site) was not a signicant predictor
of spatial distribution of Cuckoos in the studied area (the variable
was excluded because it was not signicant in the GLMM procedure, p > 0.05).
4. Discussion
We have shown that the presence of the Cuckoo is a prime
indicator of avian diversity at a local scale. To the best our best
knowledge, this is the rst test of this simple prediction, because
obviously brood parasites need the presence of hosts. However,
until now, the Cuckoo has never been considered a reliable and
simple indicator of bird species richness at a local or global scale.
Although top predators have considerable charismatic value, and
although other species with large area requirements are sometimes used as umbrella species, their general utility as bioindicators
remains uncertain and controversial (e.g. Roberge and Angelstam,
2004; Roth and Weber, 2008). Thus, selection of a better surrogate of biodiversity is a key priority in conservation biology. Our
results highlight the excellent performance of Cuckoos when used

P. Tryjanowski, F. Morelli / Ecological Indicators 55 (2015) 5258

55

Fig. 1. Relationship between Cuckoo occurrence (CUCP, upper panel) and top predators occurrence (RAPP, lower panel), and total bird species richness (biodiversity measure,
TOTBR Y-axis). The gure shows the proportion of presence/absence of, respectively, Cuckoo and top predators in each category of sampled sites classied by bird species
richness values.

Fig. 2. Spatial mismatch between the pattern of bird species richness (biodiversity surrogate measured in the eld) and predicted values of bird species richness, following
the GLM models performed on Cuckoo and top predator occurrence. The patterns were mapped using the inverse distance weighted (IDW) technique. The values of bird
species richness are represented in coloured-scale from dark violet (lowest values) to dark green (highest values). The example shown is from the 2009 breeding season, but
all breeding seasons show better pattern correspondence between species richness and predicted species richness derived from Cuckoos models (signicance was found in
a Mantel test). (For interpretation of the references to color in this gure legend, the reader is referred to the web version of this article.)

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P. Tryjanowski, F. Morelli / Ecological Indicators 55 (2015) 5258

Table 2
Results of GLMM for best models relating occurrence of cuckoos and top predators to biodiversity measures (bird species richness and land use diversity) during the years
20092012 in farmlands of Western Poland. Signicant variables are evidenced in bold.
Variables

Cuckoos (AIC: 297.3, BIC: 312.5)

Fixed effects

Estimate

SE

Top predators (AIC: 402.6, BIC: 417.8)


Estimate

SE

Species richness
Land use diversity
Intercept
Random effects
Sampled site
Year

0.210
0.130
2.871
Variance
0.014
0.001

0.036
0.045
0.717
SD
0.121
0.002

5.8
1.0
4.0
Groups
59
4

<0.0001
>0.05
<0.0001
Obs.
330
330

0.100
0.058
2.149
Variance
0.065
0.076

0.033
0.029
0.526
SD
0.256
0.276

2.992
1.250
4.087
Groups
59
4

<0.0001
>0.05
0.05
Obs.
330
330

as indicators of bird taxonomic diversity. In this study, the predictive capacities of Cuckoos as indicators of bird species hotspots
were higher than the presence of top predators and single raptor species. In contrast, the distribution of single raptor species
was for two species insufcient to be used for predictive purposes. While statistical models using the presence of top predators
showed overall reliabilities of 59%, the same models for Cuckoo
occurrence improved the reliability of BSR indicators to more than
75%, an increase of 27% for surrogate capacities compared to the
four species of raptors. We can exclude the possibility that the density of potential preferred hosts was the only contributing factor
to this superior performance of the Cuckoo because potential hosts
was not a signicant predictor of the spatial distribution of Cuckoos.
Thus other factors must be invoked.
Cuckoos were mainly present at sites with greater species richness, while raptor species, as reected by the top predator group,
were present at sites with relatively low avian species richness.
We believe that the relationship between occurrence of Cuckoo
and bird diversity can be explained as follows. The Cuckoo has coevolutionary links with other bird species resulting from strong
parasite-host interactions. From a co-evolutionary perspective, our
ndings are consistent with the hypothesis that the long-term ebb
and ow of co-evolutionary selection might be an important source
of ecological dynamics increasing biodiversity in biological communities (Thompson and Cunningham, 2002). On the other hand,
the reduced ability of predators to predict local biodiversity of birds
may be connected to diet because voles and other small mammals (not only birds) constitute an important component of the

diet of Buzzard and Kestrel (Casagrande et al., 2008; Manosa,


2003;
Redpath et al., 2001; Rooney and Montgomery, 2013; Slagsvold
et al., 2010).

The ability of Cuckoo to act as a reliable indicator of avian


diversity ts theoretical predictions about the link between brood
parasitism and biodiversity. Hochberg and van Baalen (1998) in
theoretical models suggested that defense and offense covary positively across gradients of productivity. Thus sites with higher avian
biodiversity should be characterized by higher diversity of host
races of the Cuckoo, as well as higher abundance. Our ndings
are also congruent with predictions derived from the geographic
mosaic theory of coevolution (Gomulkiewicz et al., 2007, 2000).
Diversity of birds at a local scale in agricultural landscapes is positively correlated with landscape heterogeneity, and, therefore,
the extent of edges preferred by egg laying cuckoos as vantage points for nding host nests (ien et al., 1996; Vogl et al.,
2004).
The strong relationship between the presence of Cuckoo and
avian biodiversity may also relate to recent research showing that
resident and short distance migratory host species of the Cuckoo
responded strongly to climate change by advancing their spring
arrival date, while the Cuckoo did not, which caused a temporal
mismatch in arrival time and hence breeding time (Mller et al.,
2011; Saino et al., 2009). In contrast, this was not the case for long
distance migratory hosts. The relationship between cuckoos and
avian diversity could be consistent also with these ndings. The
higher frequency of Cuckoos at sites characterized by high species
richness of birds suggests that sites with higher avian biodiversity may mitigate the effect related to temporal mismatch between
Cuckoos and some potential hosts.
Cuckoos are also common in habitats other than agro ecosystems, and we suggest that they are also investigated for their ability
to reliably indicate avian diversity. Cuckoos are widespread across
the world (Erritze et al., 2012), and we hypothesize that hotspots

Fig. 3. Differences in predictive performance of Cuckoo and top predators for biodiversity (bird species richness). The lines represent the area under the curve (AUC) that
constitutes a measure of the goodness of t of models, indicating how well they t a set of observations using the selected surrogates as predictors. The AUC were calculated
for all years separately. The values showed under the curve are the average AUC.

P. Tryjanowski, F. Morelli / Ecological Indicators 55 (2015) 5258

of cuckoos in Southeast Asia and Africa may likewise be hotspots


of avian diversity.
However, a concern remains about the use of such a simple measure as species richness as a surrogate of overall biodiversity. As
highlighted above, a means of measuring the distribution of overall biodiversity is needed in order to assess conservation priorities,
reducing the times related to sampling problems of exhaustive
surveys (Williams and Gaston, 1994). In effect, by concentrating
on areas where there is greatest need and where the payoff from
safeguard measures would also be greatest, conservationists can
respond better to the main risks to conservation of biodiversity
(Myers et al., 2000). Futhermore, species richness, often used to
dene biodiversity hotspots, is the most commonly used measure
of biodiversity because it is straightforward and intuitive. Despite
the fact that biodiversity hotspots have a prominent role in conservation biology, it remains controversial to what extent different
types of hotspot are congruent (Orme et al., 2005).
In conclusion, our ndings highlight the advantages of using
Cuckoos in ecological studies focused on biodiversity, offering an
alternative to the much used, but criticized, charismatic top
predators. The Cuckoo is characterized by attributes that facilitate
the use of this species as a bioindicator. It is a charismatic bird
that is relatively easy to count or detect from its song. Moreover,
considering the main types of relationship between local richness
species and regional species richness proposed by Gaston (2000)
(any increase in local diversity can correspond to an increase proportional or not in regional diversity), and that the methodology
used in this study is based on sampled sites by point-count, a
methodology often used also in large scale studies (regional monitoring programs), similar results can be expected for other spatial
scales.
Additionally, cuckoos represent a good candidate-species for
ordinary citizens to become involved in surveys to monitor their
arrival and presence. A recent study in France has used TV advertisements to encourage young people to volunteer to detect the
arrival of cookoos in their local area and submit the information to
a web survey. This method is proving an efcient way of collecting
high-quality data, with large savings for the public institutions
(http://www.dailymotion.com/playlist/x1yf6c yannaki missionsprintemps-2012/1#video=xpon1m) (Jiguet et al., 2012). These
kinds of stratergies can be exploited in order to nd reliable
surrogates of avian diversity, thereby reducing monitoring costs.
Acknowledgements
We thank Y. Benedetti, M. Antczak, Z. Kwiecinski, M. Hromada,
P. Szymanski and M. Tobolka for their help in the eld, as well as
two anonymous referees for constructive comments. We are also
very grateful to prof. Emma Nelson from Liverpool University, for
the English revision of the manuscript.
Appendix A. Supplementary data
Supplementary data associated with this article can be
found, in the online version, at http://dx.doi.org/10.1016/j.ecolind.
2015.03.012.
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