Ibis (2012), 154, 5–14

The impact of researcher disturbance on nest

predation rates: a meta-analysis
JUAN D. IBÁÑEZ-ÁLAMO, 1,2 * OLIVIA SANLLORENTE 1 & MANUEL SOLER 1,2
1
Departamento de Zoologı́a, Facultad de Ciencias, Universidad de Granada, E-18071 Granada, Spain
2
Grupo Coevolución, Unidad Asociada al CSIC, Universidad de Granada, E-18071 Granada, Spain

The effects of visits to nests by researchers interested in quantifying avian nesting success
have received considerable attention, as researchers have long been concerned about the
possible negative effects of their own activities on the resulting estimates. There is a
widely held view that investigator disturbance has an overall negative effect on breeding
success by increasing nest predation rates in the nests studied. However, to date no one
has statistically assessed the empirical evidence for such a relationship. We undertook a
meta-analysis of published results to assess whether researcher activities increase nest
predation in birds. We also assessed the variability in this effect in relation to the traits of
the study species and the methodology used. These analyses used data from 18 experi-
mental studies involving 25 species from six avian orders. Our results suggest that, con-
trary to the traditional view, researcher activities do not generally affect the incidence of
nest predation. Moreover, this relationship appears inconsistent among avian orders and,
surprisingly, nest survival of passerines increased weakly with researcher activities. We
also found significant positive effects of researcher activity on nest survival for species
breeding on coastal areas and for species nesting on the ground. The possible explanation
for these differences among orders and guilds could be due to different nest predator
communities. This new perspective on the effect of investigators could have important
implications for bird management and conservation, as well as for other fields of study
such as ecology and evolution, in which nest survival rates measured in the field are
widely used to test and support a range of hypotheses.
Keywords: breeding success, human perturbation, investigator activities, observer effect.

Researchers have long been concerned about
the effects of their own activities on their study
species (e.g. Johnson 1938, Harris 1964, Choate
1967, Grier 1969). The ‘uncertainty principle’
(Heisenberg 1927, Johnson 1938, Lenington 1979)
suggests that the process of collecting data in the
field could alter the results subsequently obtained.
In particular, ornithologists have long realized that
research activities could negatively affect avian
nesting success (e.g. Anderson & Keith 1980,
Cairns 1980, Pierce & Simons 1986, Boellstorff
et al. 1988). Interest in this subject increased as
this realization grew, and researchers subsequently
studied it and proposed several methods to mini-
*Corresponding author.
Email: jia@ugr.es
mize such effects (e.g. Armstrong 1993, Rodway
et al. 1996). The conception of a negative effect of
investigation on nest survival rates quickly perme-
ated the scientific community and was included as
an issue of special concern in the ethical policy of
some research institutions. Götmark (1992) pub-
lished an extensive narrative review on the topic in
which he concluded that in 49% of the studies
reported to that date, research activities had led to
a reduction in nesting success. This and other stud-
ies established in the scientific community the con-
ception that investigator disturbance had a general
negative effect on avian breeding success by
increasing nest predation rate of the nests visited
(Götmark 1992, Carney & Sydeman 1999).
Many studies on the subject have been
published since then, most of them reporting no

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Ibis ª 2011 British Ornithologists’ Union
6 J. Ibáñez-Álamo et al.
overall effect (e.g. Schaub et al. 1992, Cotter &
Gratto 1995, Lloyd et al. 2000, Bêty & Gauthier
2001, Verboven et al. 2001) or, surprisingly, even a
positive effect of nest visiting by researchers on
nesting success (e.g. Mayer-Gross et al. 1997,
Ortega et al. 1997, Weidinger 2008, Ibáñez-Álamo
& Soler 2010). This positive effect has been
explained by the high sensitivity of nest predators
and their avoidance of research activities. More-
over, Nisbet (2000) suggested that published stud-
ies systematically overstate the adverse effects of
human disturbance. However, these findings
seemed to go unnoticed and the scientific collec-
tive still promotes the traditional idea that
researchers have negative effects on the reproduc-
tive success of birds. To date, no one has inves-
tigated this overall empirical evidence with
meta-analytical procedures, a methodology that
has been highly recommended for such investiga-
tions (Stewart 2010). Therefore, a quantitative
synthesis is needed to clarify how researchers’
activities impact on the nest survival rates of their
study populations.
In addition, it would also be of use to assess
how particular species traits influence the relation-
ship between research activities and nest predation
rates. For example, there are marked differences
between habitats in the community of nest preda-
tors. Mammals are generally more important nest
predators in grasslands and coastal areas than in
forested landscapes (Richardson et al. 2009), but
mammals are the group of nest predators most
sensitive to human activities (MacIvor et al. 1990,
Miller & Hobbs 2000, Sinclair et al. 2005), so birds
nesting in habitats where mammals are the main
nest predators might be expected to be less nega-
tively affected by research activities. Similarly,
nesting on the ground could also influence the
effects of research disturbance, as ground nest pre-
dators are mainly mammals (Richardson et al.
2009). Coloniality is another trait that could
potentially increase nest predation through investi-
gator disturbance (Johnson 1938, Götmark 1992),
because a visit to a colony can result in disturbance
to many birds simultaneously, favouring predation
by opportunistic nest predators (sometimes con-
specifics).
Previous narrative reviews have also suggested
that each avian taxon could be affected differently
by research activities (Götmark 1992, Carney &
Sydeman 1999) because of their particular traits
(e.g. Passeriformes are mainly territorial and nest in
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Ibis ª 2011 British Ornithologists’ Union
trees, whereas Charadriiformes are principally
colonial and ground nesters). Therefore, it would
be interesting to explore this possibility statistically
and assess whether some orders are more affected
by research activities than others. This approach
would help to identify those groups that might be
most vulnerable to research activities.
The different field methods used to monitor
nest success could also have significant impacts on
disturbance and reproductive performance of birds
(e.g. Tremblay & Ellison 1979, Fetterolf 1983,
Boellstorff et al. 1988, Brown & Morris 1995,
Rodway et al. 1996). Therefore, it is important to
assess whether our methodological procedures
have an overall effect on the reproductive success
of birds and, if so, to identify methods that have
the smallest impact.
In this study, we use meta-analytical procedures
to evaluate the evidence of a negative association
between investigator disturbance and nest preda-
tion. We also assess whether there is variability
among avian orders in research impact, test for
different traits that could influence this effect (e.g.
coloniality), and assess the effect of the different
methodologies used to assess nest survival.
METHODS
Literature search and selection of
published studies
We first checked all articles included in Götmark’s
review (1992), assuming that this review had
included all the usable studies published prior to
1992. We then searched the Web of Science data-
base for all articles related to the subject using
‘research*’, ‘investigat*’, ‘perturbation’, ‘distur-
bance’ and ‘nest predation’ as key words. Litera-
ture cited in relevant papers was also examined. In
this review, we selected only experimental studies
and excluded those using anecdotal data or report-
ing the effect of research activities without a
well-designed experiment (i.e. not assigning exper-
imental and control nests randomly). We based the
review on papers focused on nest predation, which
has been determined as the main cause of reduc-
tion of nesting success due to investigator distur-
bance (Götmark 1992). Only studies involving
natural nests were included in the review, as it has
been shown that artificial nests can result in
misleading findings with respect to nest predation
(Weidinger 2001, Zanette 2002, Moore & Robinson
 Impact of researchers on nest predation 7

2004). Our search found 101 articles. However,
the majority were not experimental studies
designed to test the effect of researcher activity,
and only 18 studies involving 25 different bird
species were considered to meet all criteria and
included in the analyses (Tables 1 and 2). We
found three cases in which two different studies
offered similar information for the same species
(Eider Somateria mollissima, Blackbird Turdus
merula and Mourning Dove Zenaida macroura). In
these cases, we chose the best designed study (i.e.
that considering the potential effect of territorial
predators).
The following data were extracted from the
selected studies: (1) author; (2) study species; (3)
number of depredated and successful nests under
the high perturbation treatment; (4) number of
depredated and successful nests under the low ⁄
non-perturbation treatment; (5) habitat (grassland,
coast or forest); and (6) method of study (fre-
quency of visits, visit ⁄ non-visit or touched ⁄
untouched). The frequency of visits method
consisted of visiting experimental nests more
frequently than controls, but always involved at
least one visit to the latter. In contrast, the visit ⁄
non-visit method consisted of visiting the experi-
mental nests several times but using remote obser-
vations to determine the fate of control nests (i.e.
using binoculars). The touched ⁄ untouched method
consisted of the same regime of visits to both treat-
ments, but one involved manipulating (touching)
the nest contents, whereas the other only involved
observation of the nest when visited. When possi-
ble, we used or transformed daily predation rates
into nest predation rates (i.e. Schaub et al. 1992)
to extract the number of predated and successful
nests for each treatment. We classified all species
as colonial or solitary, and nesting on the ground or
above it according to the information given in the
studies when possible, and using published compi-
lations (e.g. Cramp 1978–1994, Del Hoyo et al.
1992–2010) when this information was absent
from the original sources (Table 1).
Meta-analytical procedures
To assess the effect of investigator disturbance on
nest predation rate, we conducted a phylogenetic

Table 1. Species considered in the meta-analysis, and classifications of avian order, coloniality (C colonial, S solitary), nest location
(G ground nester species, AG species nesting above ground) and habitat type.

Scientific name English name Avian order Coloniality Nest location Habitat

Anser caerulescens Snow Goose Anseriformes C G Grassland

Aphelocoma coerulescens Florida Scrub Jay Passeriformes S AG Forest
Calcarius ornatus Chestnut-collared Longspur Passeriformes S G Grassland
Calidris alpina Dunlin Charadriiformes S G Coast
Carduelis cannabina Common Linnet Passeriformes S AG Forest
Carduelis chloris European Greenfinch Passeriformes S AG Forest
Catharus guttatus Hermit Thrush Passeriformes S AG Forest
Charadrius alexandrinus Kentish Plover Charadriiformes S G Coast
Charadrius melodus Piping Plover Charadriiformes S G Coast
Eremopterix verticalis Grey-backed Sparrow-Lark Passeriformes S G Grassland
Fratercula arctica Atlantic Puffin Charadriiformes C G Coast
Fringilla coelebs Common Chaffinch Passeriformes S AG Forest
Lagopus muta Rock Ptarmigan Galliformes S G Grassland
Larus delawarensis Ring-billed Gull Charadriiformes C G Coast
Prunella modularis Dunnock Passeriformes S AG Forest
Pygoscelis adeliae Adelie Penguin Sphenisciformes C G Coast
Pyrrhula pyrrhula Eurasian Bullfinch Passeriformes S AG Forest
Somateria mollissima Common Eider Anseriformes C G Grassland
Sylvia spp. Warbler Passeriformes S AG Forest
Troglodytes troglodytes Eurasian Wren Passeriformes S AG Forest
Turdus merula Common Blackbird Passeriformes S AG Forest
Turdus migratorius American Robin Passeriformes S AG Forest
Turdus philomelos Song Thrush Passeriformes S AG Forest
Vanellus vanellus Northern Lapwing Charadriiformes C G Grassland
Zenaida macroura Mourning Dove Columbiformes S AG Forest

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8 J. Ibáñez-Álamo et al.

Table 2. Classifications based on method of study (FqV frequency of visits, V ⁄ NV visit ⁄ non-visit procedure, T ⁄ UT
touched ⁄ untouched), sample size and effect size (calculated as log odds ratio, LOR) for each species considered for the meta-
analysis.

Method of Sample Effect

Scientific name English name study size size (LOR) Sources

Anser caerulescens Snow Goose FqV 383 0.179 Bêty and Gauthier (2001)
Aphelocoma coerulescens Florida Scrub Jay FqV 76 )0.088 Schaub et al. (1992)
Calcarius ornatus Chestnut-collared Longspur FqV 35 )0.775 O’Grady et al. (1996)
Calidris alpina Dunlin FqV 203 )0.442 Thorup (1995)
Carduelis cannabina Common Linnet FqV 45 0.453 Mayer-Gross et al. (1997)
Carduelis chloris European Greenfinch FqV 52 0.677 Mayer-Gross et al. (1997)
Catharus guttatus Hermit Thrush V ⁄ NV 29 )0.898 Martin and Roper (1988)
Charadrius alexandrinus Kentish Plover FqV 31 )2.138 Domı́nguez and Vidal (2003)
Charadrius melodus Piping Plover V ⁄ NV 22 )2.000 MacIvor et al. (1990)
Eremopterix verticalis. Grey-backed Sparrow-Lark FqV 145 )0.152 Lloyd et al. (2000)
Fratercula arctica Atlantic Puffin FqV 360 0.714 Rodway et al. (1996)
Fringilla coelebs Common Chaffinch FqV 32 )2.281 Mayer-Gross et al. (1997)
Lagopus muta Rock Ptarmigan V ⁄ NV 44 )0.197 Cotter and Gratto (1995)
Larus delawarensis Ring-billed Gull FqV 123 0.042 Brown and Morris (1994)
Prunella modularis Dunnock FqV 85 )0.950 Mayer-Gross et al. (1997)
Pygoscelis adeliae Adelie Penguin V ⁄ NV 227 0.899 Giese (1996)
Pyrrhula pyrrhula Eurasian Bullfinch FqV 23 1.842 Mayer-Gross et al. (1997)
Somateria mollissima Common Eider FqV 414 0.326 Götmark and Åhlund (1984)
Sylvia spp. Warbler FqV 37 0.336 Mayer-Gross et al. (1997)
Troglodytes troglodytes Eurasian Wren FqV 53 0.068 Mayer-Gross et al. (1997)
Turdus merula Common Blackbird FqV 88 )1.271 Ibáñez-Álamo and Soler (2010)
Turdus migratorius American Robin T ⁄ UT 156 )1.413 Ortega et al. (1997)
Turdus philomelos Song Thrush FqV 224 )0.359 Mayer-Gross et al. (1997)
Vanellus vanellus Northern Lapwing V ⁄ NV 321 0.258 Galbraith (1987)
Zenaida macroura Mourning Dove FqV 119 0.106 Nichols et al. (1984)

A negative effect size indicates that nest predation is lower when research activities are higher.

meta-analysis using METAWIN 2.0 (Rosenberg et al.
2000) and PHYLOMETA 1.0 (Lajeunesse 2009). We
selected this type of meta-analysis because it con-
siders the phylogenetic relationships of taxa and is
recommended when data can be phylogenetically
structured (Lajeunesse 2009). Given that our units
of analysis – the species – are phylogenetically
related, and thus cannot be considered indepen-
dent, it is necessary to control for this potential
bias. The phylogenetic meta-analysis chosen avoids
this problem, as it takes into account the phyloge-
netic relationships of the species and thus accounts
for the non-independence. We chose a 2 · 2 con-
tingency table meta-analysis because the majority
of studies only presented two levels of disturbance
(i.e. high or low). There were more than two cate-
gories of disturbance only in three studies. In these
cases, we chose the two categories that better
represented investigator activities (i.e. the most
frequent procedure used generally for studying the
species in question). We used METAWIN 2.0 to
estimate the logs odds ratio (LOR) for each study
(Table 2). We chose LOR as an association mea-
sure to enable relative comparisons across species,
rather than using absolute nest success of each
species.
Once we obtained the effect sizes, we used
PHYLOMETA 1.0 to undertake the categorical meta-
analyses to test for the effect of the different
variables considered. Random effects models in
meta-analysis are more realistic than fixed effects
models because they use both within- and
between-study variability (Hedges & Vevea 1998);
thus, we used random effects models for our meta-
analyses. We assessed the effect of avian order and
the traits nest type, coloniality and habitat type
(grassland, forested area or coastal area). We also
tested, using a categorical meta-analysis, for differ-
ences in research disturbance due to the methodo-
logical approaches of each study. The sample size
was 25 study-species combinations for all analyses
except for that including avian order and method-
ologies. The former was reduced to 20 because
there was a unique representative for Galliformes

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 Impact of researchers on nest predation 9

(Lagopus muta), Columbiformes (Zenaida macro-

ura) and Sphenisciformes (Pygoscelis adeliae) and
two for Anseriformes (Anser caerulescens and So-
materia mollissima). Analysis of methodologies was
reduced to 24 because there was one methodologi-
cal category (touched ⁄ untouched) with only one
study (Tables 1 and 2). Groups with only one
value cannot be computed in a categorical meta-
analysis, but because it is also very difficult to draw
meaningful conclusions from small groups too, we
decided to use only groups with n ‡ 5.
We calculated by hand the I2 statistic (following
Higgins et al. 2003), which describes the percent-
Figure 1. Normal quantile plot comparing the standard normal
age of variation across studies that is due to hetero-
distribution with that of the standardized effect size (LOR) of
geneity rather than chance. Higgins and Thompson the 25 studies considered in the meta-analysis.
(2002) proposed that percentages of around 25, 50
and 75% would represent low, medium and high
heterogeneity, respectively. Therefore, a high value
of this statistic (> 75%) implies that the majority
of the variability of our data is caused not by sam-
pling error but by true heterogeneity between
studies. On the one hand, a high value of the I2
statistic justifies the use of a random effects model;
on the other hand, it implies that explanatory vari-
ables other than the one used in that analysis are
responsible for the variation in LOR. The I2 statis-
tic is recommended rather than the Q statistic
because it does not depend upon the number of
studies considered (Higgins & Thompson 2002,
Higgins et al. 2003).
A common concern when conducting a meta-
analysis is the potential for publication bias (the
selective publication of articles showing certain
types of results) because it can distort the results
of the review (Rosenberg et al. 2000). The linear
shape obtained in the normal quantile plot implies
that the distribution of our effect sizes is similar to
the standard normal distribution and suggested
little bias in the studies included in our review
(Fig. 1). Thus, we concluded that studies showing Figure 2. Maximum likelihood phylogenetic tree of the species
significant effects have not been selectively pub- considered in the meta-analysis. For those species for which
lished in comparison with those finding no effects. Cyt b data were not available, we used information from other
related species within the same genus: 1Anser canagica, 2Syl-
via communis, 3Charadrius semipalmatus, 4Charadrius vocife-
Phylogenetic data rus and 5Vanellus chilensis.

We searched GenBank for the sequences needed to

construct a phylogeny of the species obtained in
the literature search. Cyt b was the gene chosen as
it resolved very well the topology of taxa following
published molecular phylogenies (e.g. Ericson &
Johansson 2003, Dong et al. 2010). Moreover,
sequences for this gene were available for the
majority of the species included in the selected
studies (80% of the 25 bird species). For those spe-
cies for which Cyt b data were not available, we
used information from other related species within
the same genus (Fig. 2). All sequences were
aligned with CLUSTALW using BIOEDIT version 5.0.6

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Ibis ª 2011 British Ornithologists’ Union
10 J. Ibáñez-Álamo et al.
(Hall 1999). The most suitable substitution model
was estimated using MODELTEST 3.7 (Posada &
Crandall 1998), which compares 56 models of
DNA substitution. Under the Akaike information
criterion, the transversion model with invariable
sites and gamma distribution (TVM+I+G) was
determined to be the best model for these data.
Then, maximum likelihood (ML) trees were pro-
duced with PAUP* version 4.0 b10 (Swofford 2003)
and node support was assessed with 100 bootstrap
replicates. The phylogenetic tree obtained follow-
ing this procedure is shown in Figure 2 and fits
very well with established phylogenies (e.g. Davis
2008).
RESULTS
In general, investigator activities did not signifi-
cantly affect nest predation rates of birds
(Z1 = 0.68, P = 0.41, mean effect sizes ±
sd = 0.194 ± 0.047, I2 = 86%). However, when
analysed by avian order, Passeriformes showed a
marginally significant effect of researcher distur-
bance (Z1 = 3.59, P = 0.058, effect size =
)0.397 ± 0.056, I2 = 64%). A negative value of
the effect size indicates that the odds of a nest
being predated for the treatment group (high
investigator disturbance) are less than that of the
control group (low investigator disturbance), sug-
gesting a negative effect of researcher activities on
nest predation. Charadriiformes (the only other
order with sufficient sample size) did not show sig-
nificant effects of researcher activities (Z1 = 0.78,
P = 0.38, effect size = 0.231 ± 0.110, I2 = 66%).
In relation to species traits of the species, we
also found some positive impacts of researcher vis-
its on breeding success. There was a significant neg-
ative effect of researcher activity on nest predation
of ground nesters (Z1 = 7.80, P < 0.01, effect
size = )0.529 ± 0.055, I2 = 97%), but not for
those species that nest above the ground
(Z1 = 0.04, P = 0.84, effect size = )0.047 ± 0.066,
I2 = 90%). Coloniality appeared not to modify the
impact of investigator activities on nest predation
(Z1 = 2.74, P = 0.10, effect size = )0.337 ± 0.047,
I2 = 57%) or for solitary species (Z1 = 1.34,
P = 0.25, effect size = 0.223 ± 0.079, I2 = 83%).
There was a significant negative effect of researcher
disturbance on nest predation rates of species
breeding in coastal areas (Z1 = 11.01, P < 0.001,
effect size = )0.794 ± 0.098, I2 = 95%), but not
for those nesting in grasslands (Z1 = 0.01,
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Ibis ª 2011 British Ornithologists’ Union
P = 0.97, effect size = 0.008 ± 0.095, I2 = 64%) or
forested areas (Z1 = 0.04, P = 0.84, effect
size = )0.047 ± 0.066, I2 = 90%).
Studies using frequency of visits as an estimate
of researcher disturbance were significantly more
likely to find negative effects of investigator distur-
bance on predation rates (Z1 = 4.05, P = 0.04,
effect size = )0.373 ± 0.043, I2 = 94%), but not
those using a visit ⁄ non-visit procedure (Z1 = 0.03,
P = 0.87, effect size = )0.055 ± 0.152, I2 = 71%).
According to the classification of I2 values
proposed by Higgins and Thompson (2002), the
majority of the groups had high heterogeneity,
justifying the use of a random effects model, and
the use of several predictor variables (avian order,
habitat, coloniality, nest-site and method of study)
to identify causes of such variability.
DISCUSSION
Overall effects and differences between
avian orders
Contrary to previous reviews, our meta-analysis
suggests that there is no general effect of investiga-
tor disturbance on nest predation in the selected
studies. Carney and Sydeman (1999) suggested the
existence of publication bias favouring the publica-
tion of studies that find significant effects, but our
results do not support this statement (Fig. 1).
Our results show marked differences among
avian orders. For example, Charadriiformes did not
show a significant increase in nest predation due to
research perturbation (n = 6 species), as previously
reported (Götmark 1992, Carney & Sydeman
1999, but see Nisbet 2000). Moreover, Passerifor-
mes were not only less negatively affected, but per-
haps even favoured by the investigator’s presence,
although this effect was only marginally significant
(P = 0.058, n = 14 species). A recent meta-analysis
of camera effects on avian nesting success using
mainly passerines obtained similar results (Richard-
son et al. 2009). Contrasting findings between
avian orders could be due to the different sensitiv-
ity of predators to research activities, a possibility
largely ignored until recently (Sutherland 2007).
Charadriiformes are thought to be predated mainly
by other birds such as corvids or other Charadrii-
formes (e.g. Burger 1981), which are the least
affected by investigator disturbance among the
community of nest predators (e.g. Strang 1980,
Götmark & Åhlund 1984, Götmark 1992).

Although passerines usually have a broader com-
munity of nest predators, a partial reduction in
predation (i.e. due to mammals) could be enough
to increase the breeding success of species of this
order (e.g. Ibáñez-Álamo & Soler 2010). The posi-
tive effects of research activities on avian breeding
success could be explained as a consequence of
mammalian nest predators avoiding those places
more frequently visited by researchers (MacIvor
et al. 1990, Armstrong 1993, Ibáñez-Álamo & Soler
2010). However, the mechanism underpinning this
avoidance is not clear. Possibly mammals avoid
preferentially those areas with fresh human odours,
or simply avoid direct contact with humans.
It should be noted that the database in which
we have based our analyses was somewhat biased
by an over-representation of Passeriformes (56% of
species considered; Table 1). Nevertheless, the use
of the phylogenetic meta-analysis, which makes
each species independent phylogenetically, pre-
vents or at least considerably reduces this effect.
Results concerning avian order variability, and
especially the weakly positive effect for Passerifor-
mes, could have important implications for
research. Passerines have been widely used to test
general hypotheses in several fields such as ecology
or evolution (e.g. life-history theory; Martin 2004).
Therefore, the conclusions of those studies should
be viewed with caution, given the possibility that
their findings do not reflect the natural situation.
The fact that this effect may be positive suggests
that significant results involving nest predation
would be more difficult to detect, as nest predation
pressure may be relaxed in study populations.
Researchers should therefore be aware that such
effects on nest predators in their study sites may
affect the results of nest predation studies.
Influence of species traits and methods
of study on disturbance effects
Certain traits of the studied species could also
modify research impacts on nest predation. The
activities of researchers appeared significantly to
reduce nest predation of species nesting on the
ground (n = 12 species), but not of those nesting
above it (n = 13 species). This suggests that the
impact of disturbance on predators of ground nest-
ers is more important than that of species nesting
above the ground. Mammals are the main nest
predator of ground nesters (Richardson et al.
2009) and they are the group most sensitive to
Impact of researchers on nest predation 11
human presence (MacIvor et al. 1990, Armstrong
1993, Miller & Hobbs 2000, Sinclair et al. 2005,
Ibáñez-Álamo & Soler 2010). Consequently,
researchers could increase the breeding success of
ground nesters through their presence in the field.
In contrast, species nesting above the ground have
a wider variety of nest predators (Richardson et al.
2009). Although some would be disturbed by
researchers, others (e.g. corvids) would not, or
could even be attracted by the presence of humans
(Strang 1980, Götmark & Åhlund 1984), which
makes it difficult to obtain a clear response for this
group of species.
In relation to coloniality, we did not find any
significant effect of research activities using a statis-
tical approximation, contrasting with previous
findings (Götmark 1992).
We also found that species breeding in coastal
areas were significantly favoured by researchers
through a reduction of nest predation (n = 6 spe-
cies), whereas we failed to find any significant
effect for those species nesting in grasslands (n = 6
species) or forested areas (n = 13 species). Studies
on the effects of investigator disturbance on avian
breeding success originally focused on coastal spe-
cies (e.g. Harris 1964, Tremblay & Ellison 1979),
finding negative impacts on nesting success due to
research activities. However, many of them
included only anecdotal evidence or were not
properly designed to investigate this topic
(Götmark 1992 and references within). As stated
in the introduction, we originally thought that dif-
ferences in the community of nest predators could
explain these results, but the fact that we did not
find any significant effect for those species living in
grasslands suggests other possibilities (i.e. habitat
visibility).
The high I2 values for the analyses of species
traits suggested that other variables, rather than
those considered in turn for each analysis, could
explain the variance in effect sizes between our
species. It would have been interesting to analyse
the interactions between species traits (i.e. habi-
tat · coloniality) but, to our knowledge, meta-
analytical procedures cannot implement this kind
of analysis. As stated for passerines above, some
groups of species traits are over-represented in the
database used for the analyses. Solitary species rep-
resented 80% of the cases and forested species 52%
(Table 1). Thus, conclusions drawn from those
traits (coloniality and habitat) should be regarded
with caution.
ª 2011 The Authors
Ibis ª 2011 British Ornithologists’ Union
12 J. Ibáñez-Álamo et al.
The methods used to test investigator effects
also influenced the results. Those studies compar-
ing different frequencies of visits (FqV) obtained
significantly more positive effects (n = 19 species)
than those using a visit ⁄ non-visit methodology
(V ⁄ NV; n = 5 species). These findings seem to be
due to the differences between the control treat-
ments for each procedure (low perturbation for
FqV or non-perturbation treatment for V ⁄ NV) as
nests of the high perturbation treatment of both
methodologies were visited similarly (F1,22 = 0.97;
P = 0.34; FqV = each 2.50 ± 0.21 days, V ⁄ NV =
each 3.00 ± 0.47 days). This is likely to happen
because, by visiting a nest only once or twice
(instead of not visiting it), there could be an
increase in nest predation probability as a result
(i.e. due to the absence of parents at the nest),
which will magnify the positive effects of visits
when compared with highly disturbed nests. These
results, therefore, have two interesting implica-
tions. First, they imply that the regime of visits by
researchers has positive effects on nest survival and
support the idea that birds could benefit from our
activities with a reduction in nest predation, but
only with regular visits to the nests. If we increase
our presence in the field, the probabilities of dis-
turbing nest predators from the area where the
nest is located appear higher (Ibáñez-Álamo &
Soler 2010). Secondly, our results suggest that
positive effects of visits on nest survival could
be overestimated in our analysis because the
frequency of visits method was the most com-
monly used in our sample (Table 1).
Management implications
Wildlife managers could use these results to apply
and update conservation measures. Some authors
have recommended the prohibition of research
activities in protected areas (e.g. Boellstorff et al.
1988), but wildlife managers should reconsider
this option in the light of our results. In fact, wild-
life managers could benefit from research activities,
not only by obtaining relevant information about
the focal species, but also from the potential posi-
tive effects of that investigation on the breeding
success of certain species. However, it is possible
that this reduction in nest predation will negatively
affect nest predators. Moreover, research activities
could negatively affect the focal species in other
subtle ways, such as a change in breeding density
or an increase in the level of stress that may result
ª 2011 The Authors
Ibis ª 2011 British Ornithologists’ Union
in lower fitness (Carey 2011). Therefore, managers
should evaluate carefully their main conservation
goals when granting research projects for the areas
under their supervision.
In relation to this, there is a recent trend of
studies investigating the effect of ecotourism and
recreational activities (e.g. Giese 1996, Miller &
Hobbs 2000, Taylor & Knight 2003, Nevin &
Gilbert 2005). As the work performed by
researchers seems more extreme (e.g. by capturing
or manipulating birds or visiting nests) than eco-
tourism and recreation (Carney & Sydeman 1999),
we might predict that those activities will not be
as negative, at least in relation to birds. Indeed,
there are already some papers highlighting the lack
of effects or even the positive impacts due to this
type of human activity (e.g. Lindsay et al. 2008,
Leighton et al. 2010). However, this does not dis-
claim the existence of negative impacts due to
human activities, especially in mammals (e.g.
Miller & Hobbs 2000, Reed & Merenlender 2008)
or even in birds due to other more subtle altera-
tions as commented previously.
CONCLUSIONS
Our results suggest that investigator disturbance
does not necessarily involve a negative effect on
breeding success, mediated by nest predation, as
previously assumed. Moreover, research activities
could have positive effects on nest survival in cer-
tain avian taxa, although this effect could be influ-
enced by the method of study. However, this new
perspective could have important implications in
bird management and conservation, as well as in
other fields of study such as ecology and evolution,
where passerines are widely used to test general
hypotheses. It is also important to highlight that
information on certain avian taxa and on cavity
nesters is scarce. Therefore, studies on the impact
of investigator disturbance on the breeding biology
in these taxa, and especially in cavity-nesting spe-
cies, would be of particular interest. Finally, the
effect of research activities on nest predator species
seems to have been overlooked, even though some
nest predators seem to be more sensitive to investi-
gator disturbance than the studied species. Thus, it
will be crucial for future studies to investigate the
impacts of scientific disturbance on nest predators.
P. Donald, M. Griesser, L. Lens, J. G. Martínez, A. P.
Møller, J. Reynolds and two anonymous reviewers made

useful suggestions to previous drafts. This study was par-
tially supported by the Spanish Ministry of Environment
(Project 87 ⁄ 2003) to M. Soler and by an FPU predoc-
toral grant to J. D. Ibáñez-Álamo.
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Received 23 March 2011;
revision accepted 6 October 2011.
Associate Editor: Jim Reynolds.