Insectivorous birds consume an estimated 400–500 million tons of prey annually

Abstract

In this paper, we present an estimate of the predation impact of the global population of insectivorous birds based on 103 (for the most part) published studies of prey consumption (kg ha⁻¹ season⁻¹) of insectivorous birds in seven biome types. By extrapolation—taking into account the global land cover of the various biomes—an estimate of the annual prey consumption of the world’s insectivorous birds was obtained. We estimate the prey biomass consumed by the world’s insectivorous birds to be somewhere between 400 and 500 million metric tons year⁻¹, but most likely at the lower end of this range (corresponding to an energy consumption of ≈ 2.7 × 10¹⁸ J year⁻¹ or ≈ 0.15% of the global terrestrial net primary production). Birds in forests account for > 70% of the global annual prey consumption of insectivorous birds (≥ 300 million tons year⁻¹), whereas birds in other biomes (savannas and grasslands, croplands, deserts, and Arctic tundra) are less significant contributors (≥ 100 million tons year⁻¹). Especially during the breeding season, when adult birds feed their nestlings protein-rich prey, large numbers of herbivorous insects (i.e., primarily in the orders Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, and Orthoptera) supplemented by spiders are captured. The estimates presented in this paper emphasize the ecological and economic importance of insectivorous birds in suppressing potentially harmful insect pests on a global scale—especially in forested areas.

Electronic supplementary material
The online version of this article (10.1007/s00114-018-1571-z) contains supplementary material, which is available to authorized users.

Full text

ORIGINAL PAPER
Martin Nyffeler
1
&Çağan H. Şekercioğlu
2,3
&Christopher J. Whelan
4
Received: 3 April 2018 /Revised: 8 June 2018 /A ccepted: 11 June 2018 / Published online: 9 July 2018
#
Abstract
In this paper, we present an estimate of the predation impact of the global population of insectivorous birds based on 103 (for the
most part) published studies of prey consumption (kg ha
−1
season
−1
) of insectivorous birds in seven biome types. By extrapo-
lation—taking into account the global land cover of the various biomes—an estimate of the annual prey consumption of the
world’s insectivorous birds was obtained. We estimate the prey biomass consumed by the world’s insectivorous birds to be
somewhere between 400 and 500 million metric tons year
−1
, but most likely at the lower end of this range (corresponding to an
energy consumption of ≈2.7 × 10
18
Jyear
−1
or ≈0.15% of the global terrestrial net primary production). Birds in forests account
for > 70% of the global annual prey consumption of insectivorous birds (≥300 million tons year
−1
), whereas birds in other
biomes (savannas and grasslands, croplands, deserts, and Arctic tundra) are less significant contributors (≥100 mil-
lion tons year
−1
). Especially during the breeding season, when adult birds feed their nestlings protein-rich prey, large numbers
of herbivorous insects (i.e., primarily in the orders Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, and Orthoptera)
supplemented by spiders are captured. The estimates presented in this paper emphasize the ecological and economic importance
of insectivorous birds in suppressing potentially harmful insect pests on a global scale—especially in forested areas.
Keywords Arthropods .Avifauna .Breeding season .Global impact .Insect pests .Predation
Introduction
Birds, represented by nearly 10,700 species, are found across
the world in all major terrestrial biomes. Accordingly, they
exhibit a large variety of life styles and foraging behaviors
(see Wiens 1989). While some birds depend predominantly
on plant diets, such as seeds, fruits, and nectar, others feed as
carnivores on animal prey, or as omnivores on a mixed diet of
plant/animal matter. Most bird species are insectivores that
depend for the most part on insects as prey (Losey and
Vaughan 2006;Şekercioğlu 2006a). In this paper,
Binsectivorous birds^are defined in a wider sense as the total
of all bird groups that include, at least temporarily, a consid-
erable percentage of arthropods (in particular insects and spi-
ders) in their diets (Lopes et al. 2016). Included in this defini-
tion are also omnivorous birds such as starlings (Sturnidae)
and thrushes (Turdidae) that consume large amounts of arthro-
pods in additionto other types of food (Del Hoyo et al. 2016).
The predominance of insectivory as a feeding style among
birds might be explained by the fact that insects (dominating
the land biota in terms of numbers, biomass, and diversity)
constitute the largest food base for terrestrial carnivorous an-
imals. So, for instance, social insects alone are assumed to
have a standing biomass of > 700 million tons globally
(compare Hölldobler and Wilson 1994;Sanderson1996).
Şekercioğlu (2006b) states that birds are Bimportant but
ecologically little known actors in many ecosystems.^
Communicated by: Sven Thatje
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s00114-018-1571-z) contains supplementary
material, which is available to authorized users.
*Martin Nyffeler
martin.nyffeler@unibas.ch
1
Section of Conservation Biology, Department of Environmental
Sciences, University of Basel, CH-4056 Basel, Switzerland
2
Department of Biology, University of Utah, Salt Lake
City,UT84112,USA
3
College of Sciences, Koç University, Rumelifeneri, Istanbul, Sariyer,
Turkey
4
Department of Biological Sciences, University of Illinois at Chicago,
Chicago, IL 60607, USA
The Science of Nature (2018) 105: 47
https://doi.org/10.1007/s00114-018-1571-z
The Author(s) 2018
Insectivorous birds consume an estimated 400–500 million tons
of prey annually
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Likewise, Wenny et al. (2011)stateBBirds provide many eco-
system services, which by and large are invisible and
underappreciated.^It has thus been suggested that
Bquantifying the services provided by birds is crucial to un-
derstand their importance for ecosystems and for the people
that benefit from them^(Whelan et al. 2015). While several
attempts had been undertaken to quantify the food consump-
tion of marine birds and shorebirds on a global scale (e.g.,
Wiens 1989;Brooke2004), the combined predation impact
of the world’s insectivorous birds is still unknown.
Here, we provide estimates for the annual biomass of
prey that is consumed by the global population of insectiv-
orous birds in individual biome types and worldwide based
on data from the literature. Furthermore, we present an
estimate of the standing biomass of the global population
of insectivorous birds. This study is intended as a
continuation of the papers by Nyffeler (2000)and
Nyffeler and Birkhofer (2017)—who were studying spi-
ders—to get a better understanding of the global extent to
which potentially harmful herbivorous insects are sup-
pressed by major natural enemies.
Methods
Estimate of the standing biomass of the global
population of insectivorous birds
For each of seven terrestrial biome types, the bird biomass
across the entire biome was assessed by calculating the prod-
uct of (D)×(W)×(Y), whereby D= mean bird density
(birdsha
−1
),W= mean bird b ody mass (kg fresh w eight bird
−1
),
and Y= area size of the entire biome type (ha). The mean
breeding bird densities (representing global averages) for the
various biome types were extracted from a world literature
review by Gaston et al. (2003) and are largely in agreement
with North American breeding bird densities compiled by
Terborgh (1989, page 71). Area sizes for the various biomes
were taken from Saugier et al. (2001); essentially, these values
do not differ very much from the more up to date 2010 land
cover distribution data provided by FAO (https://
ourworldindata.org/land-cover) but are more suitable for our
purposes because they are broken down into more detailed
cover classes than the latter ones allowing a more rigorous
assessment. To obtain a mean body mass for Arctic tundra
birds, an overall mean for 18 tundra-inhabiting species (see
Sokolov et al. 2012) was calculated based on data from Del
Hoyo et al. (2016). An overall mean body mass for desert
birds was calculated based on weight data for 26 species oc-
curring in Chihuahuan deserts (Gutzwiller and Barrow 2002).
Mean bird body mass values for the remaining six biome
types were gathered from the following literature sources:
Howell (1971); Karr (1971); Wiens (1973); Holmes and
Sturges (1975); Wiens and Nussbaum (1975); Kartanas
(1989); and Terborgh et al. (1990).
Summing up the seven subtotals produced an estimate
of the standing biomass of the global terrestrial avifauna.
From this, an estimate of the standing biomass of the glob-
al population of insectivorous birds was deduced, assum-
ing that ≈90% of the terrestrial bird individuals in the
temperate, boreal, and arctic zones and ≈60% in the tro-
pics are arthropod-eaters (see Assumption 1, BMethods^
section).
Estimate of the annual prey consumption
of the global population of insectivorous birds
We used a simple model involving few assumptions as is
advised in cases where a field of study is still largely un-
developed (Weathers 1983; Nyffeler and Birkhofer 2017).
Our estimate is based on mean values of prey consump-
tion ha
−1
year
−1
in the various biome types, which subse-
quently were extrapolated on a global scale. To retrieve
comparable data, all values obtained from the literature
were converted to kg fresh weight ha
−1
year
−1
. A total of
103preyconsumptionvaluesweregatheredfromthree
different information sources:
–Source 1: In 26 cases, published values of prey consump-
tion were used (see Supplementary material).
–Source 2: In 53 cases, energy demand estimates for bird
communities extracted from the scientific literature (see
Supplementary material) were converted into food con-
sumption measures. The conversions are based on an
overall average water content of arthropod prey of ≈
70% (Zandt 1997; Brodmann and Reyer 1999;Bureš
and Weidinger 2000), an energy density of animal matter
of 22.5 kJ g
−1
dry weight (Schaefer 1990), and 75% as-
similation efficiency (Wiens 1989). For details see
Supplementary material.
–Source 3: There is a lack of data regarding the food
consumption rates of bird communities in desert and
Arctic tundra biomes. We thus calculated food con-
sumption rates for bird communities in these two bi-
ome types based on estimates of daily energy expen-
diture and breeding bird densities. Energy expended
for standard metabolism (M, in kcal day
−1
)wascalcu-
lated with the equation M= 129 W
0.724
of Lasiewski
and Dawson (1967), whereby Wequals the weight of
an average sized bird in kg. Energy expended under
field conditions equals approximately 2.5 times stan-
dard metabolism (Holmes and Sturges 1975). For the
calculation of the desert biome values, cactus wren
(Campylorhynchus brunneicapillus, average body
mass = 38.9 g; Dunning 2007) was chosen as a stan-
dard bird representing this biome type, assuming a
47 Page 2 of 13 Sci Nat (2018) 105: 47
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

breedingseasonlengthof90–180 days (mean =
135 days) for deserts (Wiens 1991). In the case of the
Arctic tundra biome, snow bunting (Plectrophenax
nivalis, average body mass = 42.2 g; Dunning 2007)
was used as a standard tundra bird, whereby a breeding
season length of ≈100daysfortheArctictundrabi-
ome was assumed (Weiner and Głowaciński 1975). By
multiplying the resulting energy consumption value
for a standard bird with corresponding breeding den-
sity values taken from the literature (deserts: Austin
1970; Arctic tundra: Watson 1963; James and
Rathbun 1981; Montgomerie et al. 1983; Sokolov et
al. 2012), rough estimates of the energy consumption
for desert and Arctic tundra bird communities, respec-
tively, during the breeding season were obtained.
Subsequently, these energy consumption values were
converted into food consumption rates (the same conver-
sion factors being applied as in the previous paragraph),
which yielded 18 values fordesert and 6 valuesfor Arctic
tundra sites. For details see Supplementary material.
The 103 prey consumption values were assigned to the
following seven groups of terrestrial biomes: (1) tropical
forests, (2) temperate and boreal forests, (3) tropical
grasslands and savannas/Mediterranean shrubland, (4)
temperate grasslands (incl. meadows, pastures, old fields),
(5) cropland, (6) deserts, and (7) Arctic tundra. The data
were pooled by computing an average prey consumption
value (x
̅kg ha
−1
year
−1
) for each biome type. By multi-
plying the average prey consumption ha
−1
year
−1
with the
corresponding area size of each biome type (based on
Saugier et al. 2001), a prey consumption subtotal for each
biome type was derived. Summing up the seven subtotals
produced an estimate of the global annual prey consump-
tion by the insectivorous avifauna (Table 2). This figure
refers exclusively to arthropod prey, whereas other types
of invertebrates, such as earthworms, slugs, and snails, are
not included.
Our assessment is based on the following assumptions:
–Assumption 1: Prey consumption measures presented
in the literature for land bird communities were
downsized to the corresponding values for insectivo-
rous birds, taking into account that an estimated 90%
of all land bird individuals (and about two thirds of
all species) in the temperate, boreal, and arctic zones
are insectivores during the breeding season, whereas
≈60% of all individuals (and 62% of all species) in
the tropics are insectivores. The figure of 60% has
also been chosen for non-tropical desert habitats
(see Supplementary material). The figure of 90% for
the Palearctic birds has been calculated based on pop-
ulation size/diet composition data for 422 bird species
presented in the data base BBirds of Switzerland^of
the Swiss Ornithological Institute Sempach; it can be
considered to be representative for the European
temperate/cold regions (see http://www.vogelwarte.
ch/en/birds/birds-of-switzerland/). A similarly high
proportion of all breeding land bird individuals in
the Nearctic realm are insectivores (calculated based
on data presented by Wiens 1973;Wiensand
Nussbaum 1975,Holmesetal.1986; and others).
Thefigureof≈60% for tropical birds is a rough es-
timate based on various sources (see Karr 1971,1975;
Poulin et al. 1994; Poulin and Lefebvre 1996;Leigh
1999;Sakai2002; Tscharntke et al. 2008; Maas et al.
2015; Sam et al. 2017).
–Assumption 2: The breeding season diets of the avi-
fauna in temperate forests and in some temperate
grasslands are composed of ≥75% arthropods
(Głowaciński et al. 1984) and those in agricultural
areas of ≈95% arthropods (Jenny 1990;Jeromin
2002;Gilroyetal.2009). The diets of desert birds
are made up, on average, of ≈85% arthropods (e.g.,
Beal 1907). Accordingly, the food consumption
values for insectivorous birds of these biomes were
multiplied by a factor of 0.75, 0.95, and 0.85, respec-
tively, to obtain arthropod consumption measures
(kg fresh weight ha
−1
season
−1
). See Supplementary
material for exceptions.
–Assumption 3: The arthropod consumption measures
for tropical biomes relate to annual totals (breeding
season plus non-breeding season; see Karr (1975);
Leigh and Smythe (1978); Reagan and Waide
(1996); Robinson et al. (2000); Sakai (2002)). By
contrast, the arthropod consumption values for tem-
perate biomes available in the literature in most cases
constitute exclusively breeding season values. The
majority of birds in temperate forests, grasslands,
and croplands as well as deserts and Arctic tundra
sites are primarily dependent on arthropod prey while
feeding their young during the breeding season (see
Wiens 1973,1977;Jenny1990; Buckingham et al.
1999;Jeromin2002; Gilroy et al. 2009). Once the
breeding season is over, many insectivorous birds
leave their temperate/cold zone breeding sites to mi-
grate to warmer areas, resulting in strongly reduced
bird densities in the breeding habitats during the non-
breeding season (Holmes and Sturges 1975;Karr
1975; Marone 1992; Scebba 2001).Atthesametime,
the vast majority of non-migratory residents, which
inhabit temperate/cold zone habitats, switch to a diet
made up largely of plant matter during the non-
breeding season (Clements and Shelford 1939;
Brown et al. 1979; Robinson and Sutherland 1997;
Buckingham et al. 1999; Renner et al. 2012).
Sci Nat (2018) 105: 47 Page 3 of 13 47
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Reduced arthropod consumption by non-migratory
birds might be explained by the reduced availability
of arthropod prey during the non-breeding season and
by the fact that vast regions located in temperate,
boreal, and polar climates are covered with a blanket
of snow for several months, making foraging for ar-
thropod prey difficult at this time. Notwithstanding
that, arthropod consumption in these biomes during
the non-breeding season continues to a limited extent
(Bruns 1960;Davies1976; Williams and Batzli 1979;
Heinrich and Bell 1995;Kirketal.1996; Michalek
and Krištín 2009;Vel’ký et al. 2011). We assume that
in vast areas of the temperate and cold regions, the
arthropod consumption ha
−1
during the entire non-
breeding season is ≈5–10% of the breeding season
value (see Holmes and Sturges 1973,1975;
Rotenberry 1980a,b;Donaldetal.2001). Therefore,
we multiplied the breeding season values for temper-
ate biomes and deserts by 0.075 to obtain the corre-
sponding non-breeding season values.
–Assumption 4: Mediterranean shrublands were classi-
fied under Btropical savannas and grasslands^because
net primary production and bird densities in these two
habitat types are similar (Gaston et al. 2003;Chapinet
al. 2011). It must be added that the area size of
Mediterranean shrublands is small (280 × 10
6
ha) rel-
ative to the global terrestrial area, and a possible error
resulting from insufficient data is likely minor.
–Assumption5: The estimates presented in this paper are
based on studies mostly conducted in the last three
decades of the twentieth century. Patterns of bird pop-
ulation decline as discussed more recently
(Şekercioğlu et al. 2002,2004) have not been taken
into account in the estimates presented here (Tables 1
and 2) because this would have exceeded the scope of
this paper owing to few estimates of bird population
declines in the twenty-first century.
Statistical analysis of annual prey consumption
in the various biomes
To determine whether prey consumption rates (kg arthro-
pods ha
−1
year
−1
) differed among biomes, we first deter-
mined that the consumption data among biomes were not
normally distributed using normal probability plots. Rather
than using a normalizing transformation, we instead per-
formed a Kruskal-Wallis one-way analysis of variance by
ranks test. The omnibus test was followed with a pairwise
multiple comparison using Dunn’s test for multiple com-
parisons of independent samples corrected for ties (Pohlert
2018). Analyses were performed with R, the programming
language (R Core Team 2018).
Results
Standing biomass of the global population
of insectivorous birds
Based on estimates of avian standing biomass in various
terrestrial biomes, we estimate the total standing biomass
of the global terrestrial avifauna to be 3981 × 10
6
kg fresh
weight (= roughly 4 million metric tons; Table 1). This
value is similar to an estimate of 5 million tons for the
global terrestrial avifauna calculated using a different ap-
proach by Alerstam (1993). Because it is assumed that ≈
90% of all land bird individuals in the temperate, boreal,
and arctic zones and ≈60% in the tropics are insectivorous
foragers (see Assumption 1, BMethods^section), it follows
that the standing biomass of the global community of in-
sectivorous birds might be on the order of ≈3 million tons
(Table 1). This value is a small fraction of the global stand-
ing biomass of other predaceous animal taxa such as spi-
ders (≈25 million tons; Nyffeler and Birkhofer 2017), ants
(≈280 million tons; Hölldobler and Wilson 1994), or
whales (16–103 million tons; Pershing et al. 2010). The
comparatively low value of the global standing biomass
of wild birds is partially explained by the fact that birds
have a very low production efficiency (i.e., low P/A-ratio).
With other words, in birds, the vast majority of the assim-
ilated energy is lost in respiration and only ≈1–2% is con-
verted to biomass (see Golley 1968;HolmesandSturges
1975; Humphreys 1979).
Prey consumption rates of insectivorous birds
in the various biomes
Prey consumption rates (kg arthropods ha
−1
year
−1
)varied
significantly among biomes (Kruskal-Wallis chi-squared =
51.179, df = 6, P< 0.001; Fig. 1). A Dunn’sposthocmul-
tiple comparison test revealed that prey consumption in
tropical forests was greater than in all other biomes (all
P≤0.022). Prey consumption in temperate-boreal forests
was greater than in tundra (P< 0.001), desert (P<0.001),
and temperate grasslands (P= 0.009), but did not differ
from tropical grasslands and croplands. Prey consumption
was greater in tropical grassland and savanna than in desert
(P= 0.004) and tundra (P= 0.024). Finally, prey consump-
tion was greater in cropland than in desert (P= 0.044).
Prey consumption did not differ significantly among any
of the remaining biomes. Annual prey consumption corre-
lated positively with net primary production among bi-
omes, using NPP values from Chapin et al. (2011).
47 Page 4 of 13 Sci Nat (2018) 105: 47
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Table 2 Estimated annual consumption of arthropod prey (fresh
weight) of the global population of insectivorous birds. Values for
temperate biomes refer to residents and breeding migrants combined;
values for tropical biomes refer to residents and non-breeding migrants
combined. Not included in these calculations are the amounts of arthro-
pod prey consumed at migration stopover sites
Biome class Number of
assessments
Prey consumption
(kg ha
−1
year
−1
)
*
Area (ha) Prey consumption of
entire area (kg year
−1
)
(X)(Y)(X)×(Y)
Tropical forests
a
7 112.5 ± 9.2 1750 × 10
6
196,875 × 10
6
Temperate and boreal forests
b
44 44.1 ± 6.2 2410 × 10
6
106,281 × 10
6
Tropical grasslands and savannas/Mediterranean shrubland
c
7 15.8 ± 2.8 3040 × 10
6
48,032 × 10
6
Temperate grasslands (incl. meadows, pastures, old fields)
d
11 7.5 ± 0.9 1500 × 10
6
11,250 × 10
6
Cropland
e
8 20.9 ± 9.0 1350 × 10
6
28,215 × 10
6
Deserts
f
18 4.1 ± 0.8 2770 × 10
6
11,357 × 10
6
Arctic tundra
g
8 4.6 ± 1.3 560 × 10
6
2576 × 10
6
Global total (without ice-covered area) 103 –13,380 × 10
6
404,586 × 10
6
a
Karr (1975); Leigh and Smythe (1978); Reagan and Waide (1996); Robinson et al. (2000); Sakai (2002)
b
Tima (1957); Uramoto (1961); West and DeWolfe (1974); Holmes and Sturges (1975); Karr (1975); Alatalo (1978); Szaro and Balda (1979); Smith and
MacMahon (1981); Wiens (1989) (modified data from Wiens and Nussbaum 1975); Wiens (1989) (modified data from Weiner and Głowaciński 1975;
Głowaciński and Weiner 1980,1983); Weathers (1983); Keast et al. (1985); Solonen (1986); Kartanas (1989); Harris (1991)
c
Karr (1971); UNESCO (1979); Gillon et al. (1983)
d
Diehl (1971); Wiens (1977); Rotenberry (1980b); Smith and MacMahon (1981); Głowacińskietal.(1984); combined data Faanes (1982)/Kirk et al.
(1996)
e
Wiens and Dyer (1975); Woronecki and Dolbeer (1980); Kartanas (1989); Ferger et al. (2013)
f
Combined data Lasiewski and Dawson (1967)/Austin (1970)
g
Wielgolaski (1975); combined data Lasiewski and Dawson (1967)/Watson (1963); James and Rathbun (1981); Montgomerie et al. (1983); Sokolov et
al. (2012)
*
Values of prey kill (kg ha
−1
year
−1
) presented as x
̅
±SE
Table 1 Estimated standing biomass of the global terrestrial avifauna
(expressed as fresh weight kg). Values of mean number of birds ha
−1
(D)
in the various biome classes taken from Gaston et al. (2003), areas of the
various biome classes (Y) based on Saugier et al. (2001). Assuming that ≈
90% of the terrestrial bird individuals in the temperate, boreal, and arctic
zones and ≈60% in the tropics are arthropod-eaters (see Assumption 1,
BMethods^section), it is deduced that the biomass of the world’sinsec-
tivorous birds might be ≈3 million tons
Biome class Mean density
(birds ha
−1
)
(D)
Mean body weight
(kg bird
−1
)
(W)
Area (ha)
(Y)
Biomass across
biome (kg)
(D)×(W)×(Y)
Tropical forests 20.00 0.0320
a
1750 × 10
6
1120 × 10
6
Temperate and boreal forests 10.00 0.0270
b
2410 × 10
6
651 × 10
6
Tropical grasslands and savannas/Mediterranean shrubland 9.25 0.0340
c
3040 × 10
6
956 × 10
6
Temperate grasslands 4.00 0.0450
d
1500 × 10
6
270 × 10
6
Cropland 3.00 0.0380
e
1350 × 10
6
154 × 10
6
Deserts 1.75 0.1558
f
2770 × 10
6
755 × 10
6
Arctic tundra 2.00 0.0674
g
560 × 10
6
75 × 10
6
Global total (without ice-covered area) –– 13,380 × 10
6
3981 × 10
6
a
Terborgh et al. 1990
b
Holmes and Sturges 1975; Wiens and Nussbaum 1975
c
Howell 1971;Karr1971
d
Wiens 1973
e
Kartanas 1989
f
Gutzwiller and Barrow 2002
g
Sokolov et al. 2012; Del Hoyo et al. 2016
Sci Nat (2018) 105: 47 Page 5 of 13 47
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Estimate of the global annual prey consumption
by the insectivorous birds
Our calculation of the annual prey consumption by the global
population of insectivorous birds produced an estimate of
404,586 × 10
6
kg year
−1
(= 404.6 million tons; Table 2),
which corresponds to an energy consumption of ≈2.7 ×
10
18
Jyear
−1
(= 0.15% of the global terrestrial net primary
production of 1.782 × 10
21
Jyear
−1
(see Lieth 1973)).
This estimate (Table 2) does not include the amounts of
food consumed at stopover sites during the fall and spring
migrations. Currently, no quantitative assessments of the prey
biomass consumed at stopover sites have been published (also
see Lott et al. 2006); but considering the energy costs of ap-
proximately 10 to 20 billion birds migrating annually (see
Hahn et al. 2009; Berthold 2001;Wikelskietal.2003;
Fristoe 2015) and taking into account that the birds resting at
stopover sites only partially depend on arthropod food
(Schaub and Jenni 2000; Suthers et al. 2000), we estimate that
the amount of arthropod food they consume globally at stop-
over sites may be on the order of 3–5 million tons year
−1
.
Thus, arthropod consumption during migratory stopovers is
around 1% of the total amount of prey biomass consumed by
the global population of insectivorous birds (see Table 2).
Regarding the temperate, sub-polar, and polar climates, our
calculations (Table 2) assume that the arthropod consumption in
these climates during the non-breeding season is reduced to a
small fraction (≈5–10%) of the breeding season value (see
BMethods^). However, there are some studies which indicate
that the insectivorous activities of birds during the non-
breeding season may not always be reduced so drastically—at
least in some parts of the temperate/cold climate zones (see
Askenmo et al. 1977; Gunnarsson 1996; Kirk et al. 1996;
Vel’ký et al. 2011)—and it could therefore be argued our cal-
culations underestimate the contribution of birds as consumers
of arthropod prey during the non-breeding period (Table 2). To
address this issue, we considered two extreme scenarios. In sce-
nario 1, a minimum estimate was assessed based on the assump-
tion that the birds’diets in temperate/cold climates contain no
arthropods during the non-breeding season; in scenario 2, a max-
imum estimate was assessed by assuming that the birds’contri-
bution as arthropod consumers during the non-breeding season
in temperate/cold climates is 50% of the breeding season value.
With these assumptions, the annual prey consumption of the
world’s insectivorous birds was recalculated, producing a mini-
mum estimate of 396,041 million tons year
−1
and a maximum
estimate of 472,145 million tons year
−1
. Thus, the true value of
insect consumption presumably is somewhere in between ap-
proximately 400 and 500 million tons year
−1
,butmostlikely
at the lower end of this range as indicated in Table 2, because the
availability of arthropod prey during the non-breeding season is
greatly reduced in most areas of the temperate/cold climates.
For comparison, Alerstam (1993), using a different method,
estimated the total energy consumption of the world’slandbirds
(including arthropods, plant matter, and other food sources) to
be ≈7.5 × 10
18
Jyear
−1
. Our estimate for the world’s insectivo-
rous birds is consistent with this broader estimate. The difference
of 4.6 × 10
18
Jyear
−1
between the two estimates is mainly ex-
plained by the fact that in our estimate exclusively feeding on
arthropod prey is considered, whereas in Alerstam’s estimate,
feeding on additional food sources was assumed. Especially
during the non-breeding season, when the availability of arthro-
pod prey is strongly reduced in many places of the globe, land
birds consume large amounts of plant matter (Clements and
Shelford 1939; Brown et al. 1979; Robinson and Sutherland
1997; Buckingham et al. 1999;Renneretal.2012).
Discussion
Experimental evidence supporting our theory of high
global predation impact by insectivorous birds
Our calculations presented in Table 2imply that insectivorous
birds exert substantial predation pressure on insects and other
arthropods, especially in tropical and temperate/boreal forest
ecosystems. This is supported by a large number of experi-
mental studies conducted in a variety of habitats in different
parts of the world (see Şekercioğlu 2006a, Mäntylä et al. 2011;
Şekercioğlu et al. 2016 for reviews). Thereby, exclosure ex-
periments were used to document the impact of bird predation
Fig. 1 Box plots showing prey consumption rates
(kg arthropods ha
−1
year
−1
) in the various biomes. Different small case
letters above boxes indicate significant differences (Kruskal-Wallis test
followed by Dunn’s multiple comparison test; see text for details). High
and low whiskers indicate 90th and 10th percentiles, respectively. Tops
and bottoms of the boxes indicate 75th and 25th percentiles, respectively.
The horizontal bars withinthe boxes indicate the median, and the symbols
within the boxes indicate the mean biomass consumed
47 Page 6 of 13 Sci Nat (2018) 105: 47
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

on arthropods (Whelan et al. 2008). With this technique, it has
been proven that birds can significantly reduce the abundance
of herbivorous insects in tropical, temperate, and boreal for-
ests (Holmes et al. 1979; Gradwohl and Greenberg 1982;
Atlegrim 1989; Marquis and Whelan 1994; Gunnarsson
1996; Murakami and Nakano 2000; Strong et al. 2000;Van
Bael et al. 2003;Dunham2008; Morrison and Lindell 2012).
Exclosure experiments also show that insectivorous birds can
also have a negative effect on the abundance of herbivorous
insects in grasslands (Joern 1986;Bocketal.1992) and crop-
lands (Hooks et al. 2003; Perfecto et al. 2004; Kellermann et
al. 2008;Koh2008; Johnson et al. 2010;Maasetal.2016).
Negative effects of insectivorous birds on herbivorous in-
sects have been further demonstrated by means of dummy
caterpillar experiments in tropical and non-tropical biomes
(e.g., Maas et al. 2015;Roslinetal.2017).
Which prey taxa are killed by insectivorous birds?
Insectivorous birds eat a large variety of arthropod taxa (e.g.,
Rotenberry 1980b; Poulin et al. 1994; Dyrcz and Flinks 1995;
Gajdošand Krištín 1997;Orłowskietal.2014; Helms et al.
2016; Sam et al. 2017). Seven arthropod orders, Lepidoptera,
Coleoptera, Orthoptera, Diptera, Hemiptera, Hymenoptera, and
Araneae, however, are frequently consumed (Gajdošand Krištín
1997;Wilsonetal.1999; Develey and Peres 2000; Gámez-
Virués et al. 2007; Sam et al. 2017). In temperate forests and
agricultural habitats, caterpillars (Lepidoptera larvae) and bee-
tles (Coleoptera) are particularly common prey of insectivorous
birds (Holmes et al. 1979; Woronecki and Dolbeer 1980;Gajdoš
and Krištín 1997;Jeromin2002;Faytetal.2005; Moorman et
al. 2007; Gilroy et al. 2009; Pagani-Núñez et al. 2017), whereas
grasshoppers (Orthoptera) are usually an essential component in
the diets of grassland birds (Joern 1986;Bocketal.1992; Kobal
et al. 1998). Tropical forest and farmland birds frequently con-
sume beetles, ants, cockroaches (Blattodea), katydids
(Orthoptera), caterpillars, and spiders (Poulin and Lefebvre
1996;Şekercioğlu et al. 2002; Hooks et al. 2003;Koh2008;
Sam et al. 2017). Desert birds frequently feed on beetles, ants,
and termites (Maclean 2013). Termites are an important food
source for birds inhabiting tropical savannas (Korb and
Salewski 2000). In Arctic tundra habitats, birds consume mostly
tipulids (Diptera) and spiders (Araneae)—two arthropod groups
numerically dominating the arthropod fauna of the sparse tundra
vegetation (Holmes 1966;Custer and Pitelka 1978).
Relative contribution of different biome categories
to the global annual prey consumption
Birds in forests account for 75% of the annual prey consumption
of the world’s insectivorous birds (≈300 million tons year
−1
;
Table 2). Forests cover a large portion of the global terrestrial
surface area (41.6 million km
2
; Saugier et al. 2001),andinthese
productive and vegetatively complex habitats, birds usually
reach higher diversities (Willson 1974) and numbers ha
−1
com-
pared to non-forested areas (Gaston et al. 2003). A similar trend
of highest predation impact occurring in forested areas has been
reported for spiders (Nyffeler and Birkhofer 2017). Forest birds
feed frequently on potentially harmful caterpillar and beetle pests
(Holmes et al. 1979;Faytetal.2005;Moormanetal.2007). This
is especially true during the breeding season, when passerines
(song birds) catch large numbers of leaf-eating caterpillars to feed
them to their nestlings (Gibb and Betts 1963;Holmesetal.1979;
Gajdošand Krištín 1997; Mols and Visser 2002). At this time of
the year, caterpillars make up 20–90% of the nestling diets of
many species of insectivorous birds (Gibb and Betts 1963;
Pravosudov and Pravosudova 1996;Gajdošand Krištín 1997;
Török and Tóth 1999; Pagani-Núñez et al. 2017). Due to high
protein content and easy digestibility, caterpillars comprise an
optimal diet for nestling birds (Tremblay et al. 2005). Data sug-
gest that forest birds exert considerable predation pressure on
lepidopteran pests, such as the eastern spruce budworm
(Choristoneura fumiferana;Holmesetal.1979;Şekercioğlu
2006a). Crawford and Jennings (1989) found that birds
destroyed 84% of larval and pupal eastern spruce budworms at
low densities of this pest. The birds are most effective as natural
enemies at endemic pest densities (Holmes et al. 1979;Holmes
1990). Fayt et al. (2005) pointed out that woodpeckers (Picidae)
suppress the abundance of bark beetles (Curculionidae) in conif-
erous forest landscapes. Furthermore, forest birds at times feed
heavily on spiders, especially during the breeding season (Naef-
Daenzer et al. 2000; Pagani-Núñez et al. 2017). In Scandinavian
boreal forests, spiders are a major diet for overwintering tits
(Parus spp.), treecreepers (Certhia familiaris), and goldcrests
(Regulus regulus) (Askenmo et al. 1977; Gunnarsson 1996).
Spiders are an important food source for birds because of their
high content of taurine, an amino acid that plays a vital role in the
early development of many types of passerine birds (Ramsay
and Houston 2003;Arnoldetal.2007). The propensity for birds
to feed on spiders can reduce some positive economic impact of
avian insectivory because spiders themselves are highly benefi-
cial natural enemies of insects (Nyffeler 2000;Nyffelerand
Birkhofer 2017).Thesameistruewhenbirdsfeedonlarge
numbers of predaceous ants or odonates, as is sometimes the
case in purple martins (Progne subis) and house martins
(Delichon urbicum) (Kelly et al. 2013;Orłowskietal.2014;
Helms et al. 2016).
Birds in grasslands and savannas contributed 15% (i.e., ≈
60 million tons year
−1
; Table 2) to the global annual prey
biomass. Grasslands and savannas cover a vast area of the
globe (45.4 million km
2
; Saugier et al. 2001). Included in this
figure are 2.8 million km
2
Mediterranean shrublands. The
prey biomass ha
−1
year
−1
of bird communities in the grassland
biome is considerably lower than that in forests (Table 2;Ford
and Bell 1981; Wiens 1989). Notwithstanding that, North
American studies have shown that grassland birds at times
Sci Nat (2018) 105: 47 Page 7 of 13 47
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

exert noticeable predation pressure on grasshopper popula-
tions (Joern 1986;Belovskyetal.1990;Bocketal.1992).
Bird communities associated with agricultural areas contrib-
uted roughly 7% (i.e., ≈28 million tons year
−1
; Table 2).
Cropland covers an area of 13.5 million km
2
(Saugier et al.,
2001) Agricultural landscapes are mosaics of crop fields, shel-
terbelts, and tree-lined field roads (Kartanas 1989;Gámez-
Virués et al. 2007). In our estimates ofprey biomass ha
−1
year
−1
for croplands (Table 2), birds associated with tree-lined field
roads have been taken into account as well (compare Kartanas
1989). Although birds in the agricultural landscape are known
to feed at times heavily on potentially harmful lepidopteran and
coleopteran pests (Woronecki and Dolbeer 1980), examples of
farmland birds substantially suppressing crop pests are few,
which may be explained by the fact that crop fields are usually
inhabited/visited by birds in rather low numbers (Gaston et al.
2003), at least in temperate regions. Reports of birds suppress-
ing agricultural pests refer for the most part to studies in tropical
Table 3 Comparative estimates of the annual prey consumption (kg fresh weight ha
−1
year
−1
) of different groups of predaceous animals based on
published data
Predator type Biome class Prey biomass
a
(kg ha
−1
year
−1
)
Source
Vertebrates:
Insectivorous birds Salt marsh 545 Kale 1965
Insectivorous birds Urban areas 84–289 Falk 1976; Kartanas 1989
Insectivorous birds Tropical forests 100–176 Leigh 1999
Insectivorous birds Temperate forests 35–137 Holmes and Sturges 1975;WeinerandGłowaciński 1975;
Keast et al. 1985; Harris 1991
Insectivorous birds Tree-lined field roads 36–79 Kartanas 1989
Insectivorous birds Grasslands, crop fields 10–31 Ferger et al. 2013; Wiens and Dyer 1975
Piscivorous birds Freshwater lakes and marshes 8–49 Nilsson and Nilsson 1976; Biujse et al. 1993
Insectivorous primates Tropical forest 10–32 Sakai (2002)
Insectivorous bats Tropical forest 4 Kalka and Kalko 2006
Insectivorous bats Carlsbad Caverns national park Low
b
Combined data Tuttle 1994/BestandGeluso2003
Shrews Taiga forest 25–350 Shvarts et al. 1997
Shrews Reed swamp 6 Pelikan 1978
Hedgehogs Reed swamp 1 Pelikan 1978
Lizards Various biome types 3–9 Shelly 1986; Walter and Breckle 2013
Lizards Woodland on tropical island 85 Bennett and Gorman 1979
Salamanders Temperate forests 7 Burton and Likens 1975
Frogs Tropical forest 1–163 Stewart and Woolbright 1996; Walter and Breckle 2013
Frogs Temperate grasslands < 1–180 Breymeyer 1978; Pelikan 1993
Invertebrates:
Ants Tropical forest 21–147 Dyer 2002
Ants Temperate forest 177 Horstmann 1974
Ants Temperate grasslands 46–536 Kajak et al. 1971
Spiders Tropical coffee plantation 160–320 Robinson and Robinson 1974
Spiders Temperate forests 20–100 Nyffeler 2000; Nyffeler and Birkhofer 2017
Spiders Temperate grasslands 20–230 Nyffeler 2000; Nyffeler and Birkhofer 2017
Spiders Crop fields ≤10 Nyffeler 2000
Scorpions Arid zone 8 Shorthouse and Marples 1982
Wasps (Vespa) Temperate forest 1–8Harris1991
Robber flies (Asilidae) Tropical forest 7 Shelly 1986
Ground beetles (Carabidae) Temperate forest, cropland 20 Chauvin 1967;Schaefer1990
Rove beetles (Staphylinidae) Temperate forest 64 Schaefer 1990
Centipedes Temperate forest 100 Schaefer 1990
a
Original values adjusted when necessary by using correction factors obtained from the literature
b
Only a few kg arthropods ha
−1
year
−1
(Nyffeler, unpubl. estimate), taking into account a foraging area with a radius of ≈50 km for the Mexican free-
tailed bat (Best and Geluso 2003)
47 Page 8 of 13 Sci Nat (2018) 105: 47
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

plantations (e.g., Hooks et al. 2003;Koh2008). A classic ex-
ample of the successful avian control of a pest species comes
from tropical coffee plantations in Costa Rica, Guatemala,
Jamaica, Mexico, Panama, and Puerto Rico, where the coffee
berry borer Hypothenemus hampei—considered to be the
world’s most damaging insect pest in coffee—is successfully
controlled by insectivorous avian communities often largely
composed of wood-warblers (Parulidae) (Greenberg et al.
2000; Perfecto et al. 2004; Kellermann et al. 2008; Johnson et
al. 2010; Wenny et al. 2011;Karpetal.2013).
Birds associated with desert and tundra biomes account for
only a small percentage (each < 4%) of the global annualprey
biomass (Table 2). The low prey biomass ha
−1
year
−1
of birds
in these biome types reflects that such habitats are covered by
a sparse vegetation of low productivity supporting only low
densities of birds (see Gaston et al. 2003). Birds in desert and
tundra habitats prey exclusively on non-pest arthropods dur-
ing their occurrence in these biomes which renders them in-
significant from the perspective of economic ornithology
(Holmes 1966; Custer and Pitelka 1978;Maclean2013).
Concluding remarks
For the first time, the predation impact of the insectivorous
birds has been quantified on a global scale. The global energy
consumption by the insectivorous birds in the form of arthro-
pod prey is substantial (an estimated ≈2.7 × 10
18
Jyear
−1
).
Annually, the global population of insectivorous birds con-
sumes as much energy as a megacity the size of New York
(≈2.8 × 10
18
Jyear
−1
, in 2011; Kennedy et al. 2015).
To fulfill these huge energy requirements, the insectiv-
orous birds capture billions of potentially harmful herbiv-
orous insects and other arthropods. Only few other preda-
tor groups, such as spiders and entomophagous insects, can
keep up with the insectivorous birds in their capacity to
suppress herbivorous insect populations in a variety of bi-
omes (Table 3;DeBachandRosen1991;Nyffelerand
Birkhofer 2017). Other predator groups like bats, primates,
shrews, hedgehogs, frogs, salamanders, and lizards appar-
ently are less effective natural enemies of herbivorous in-
sects (Table 3). Although some of these latter predator
groups may exert high predation pressure in a particular
biome type (e.g., lizards on tropical islands; see Bennett
and Gorman 1979), these same groups are much less effec-
tive in other biomes so that their global impact cannot
compare to that of spiders, entomophagous insects, or in-
sectivorous birds. The global predation impact of the in-
sectivorous birds (between 400 and 500 million tons year
−1
)
is approximately of the same order of magnitude as that of
the spiders (between 400 and 800 million tons year
−1
;see
Nyffeler and Birkhofer 2017).
Acknowledgments We are grateful to Steffen Hahn and Lukas Jenni
(both Swiss Ornithological Institute Sempach) and Franz Bairlein
(Institute of Avian Research BVogelwarte Helgoland,^Germany) for pro-
viding us with expert knowledge needed to roughly estimate the food
consumption by migrant birds at stopover sites. We also wish to thank
Thomas Alerstam (Lund University), James Van Remsen (Louisiana
State University), andthree anonymous reviewers for their valuable com-
ments on earlier drafts.
Open Access This article is distributed under the terms of the Creative
Commons Attribution 4.0 International License (http://
creativecommons.org/licenses/by/4.0/), which permits unrestricted use,
distribution, and reproduction in any medium, provided you give
appropriate credit to the original author(s) and the source, provide a link
to the Creative Commons license, and indicate if changes were made.
References
Alatalo RV (1978) Bird community energetics in a boreal coniferous
forest. Holarct Ecol 1:367–376
Alerstam T (1993) Bird migration. Cambridge University Press,
Cambridge, UK
Arnold KE, Ramsay SL, Donaldson C, Adam A (2007) Parental prey
selection affects risk-taking behaviour and spatial learning in avian
offspring. P Roy Soc Lond B Bio 274:2563–2569
Askenmo C, Von Brömssen A, Ekman J, Jansson C (1977) Impact of
some wintering birds on spider abundance in spruce. Oikos 28:90–
94
Atlegrim O (1989) Exclusion of birds from bilberry stands: impact on
insect larval density and damage to the bilberry. Oecologia 79:136–
139
Austin GT (1970) Breeding birds of desert riparian habitat in southern
Nevada. Condor 72:431–436
Beal FEL (1907) Birds of California inrelation to the fruit industry. Part I.
US Dept Agric Biol Survey Bull 30:1–100
Belovsky GE, Slade JB, Stockhoff BA (1990) Susceptibility to predation
for different grasshoppers: an experimental study. Ecology 71:624–
634
Bennett AF, Gorman GC (1979) Population density and energetics of
lizards on a tropical island. Oecologia 42:339–358
Berthold P (2001) Bird migration: a general survey. Oxford University
Press
Best TL, Geluso KN (2003) Summer foraging range of Mexican free-
tailed bats (Tadarida brasiliensis mexicana) from Carlsbad Cavern,
New Mexico. Southwest Nat 48:590–596
Biujse AD, Van Eerden MR, Dekker W, Van Densen WLT (1993)
Elements of a trophic model for Ijsselmer (The Netherlands), a shal-
low eutrophic lake. In: Christensen V, Pauly D (eds) Trophic models
of aquatic ecosystems. ICLARM, Manila, Philippines, pp 90–94
Bock CE, Bock JH, Grant MC (1992) Effects of bird predation on grass-
hopper densities in an Arizona grassland. Ecology 73:1706–1717
Breymeyer A (1978) Analysis of the trophic structure of some grassland
ecosystems. Pol Ecol Stud 4:55–128
Brodmann PA, Reyer HU (1999) Nestling provisioning in water pipits
(Anthus spinoletta): do parents go for specific nutrients or profitable
prey? Oecologia 120:506–514
Brooke MDL (2004) The food consumption of the world’sseabirds.P
Roy Soc Lond B Bio (Supp) 271:S246–S248
Brown JH, Reichman OJ, Davidson DW (1979) Granivory in desert
ecosystems. Annu Rev Ecol Evol S 10:201–227
Bruns H (1960) The economic importance of birds in forests. Bird Study
7:193–208
Sci Nat (2018) 105: 47 Page 9 of 13 47
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Buckingham DL, Evans AD, Morris AJ, Orsman CJ, Yaxley R (1999)
Use of set-aside land in winter by declining farmland bird species in
the UK. Bird Study 46:157–169
BurešS, Weidinger K (2000) Estimation of calcium intake by Meadow
Pipit nestlings in an acidified area. J Avian Biol 31:426–429
Burton TM, Likens GE (1975) Energy flow and nutrient cycling in sala-
mander populations in the Hubbard Brook Experimental Forest,
New Hampshire. Ecology 56:1068–1080
Chapin FS, Matson PA, Vitousek PM (2011) Principles of terrestrial
ecosystem ecology, 2nd edn. Springer, New York
Chauvin R (1967) L’univers des insects. Arnoldo Mondadori, Milan
Clements F, Shelford V (1939) Bio-ecology. John Wiley and Sons, New
York
Crawford HS, Jennings DT (1989) Predation by birds on spruce bud-
worm Choristoneura fumiferana: functional, numerical, and total
responses. Ecology 70:152–163
Custer TW, Pitelka FA (1978) Seasonal trends in summer diet of the
Lapland Longspur near Barrow, Alaska. Condor 80:295–301
Davies NB (1976) Food, flocking and territorial behaviour of the pied
wagtail (Motacilla alba yarrellii Gould) in winter. J Anim Ecol 45:
235–253
DeBach P, Rosen D (1991) Biological control by natural enemies, 2nd
edn. Cambridge University Press, Cambridge, UK
Del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (2016)
Handbook of the birds of the world alive. Lynx Edicions,
Barcelona http://www.hbw.com/ (accessed 16 June 2017)
Develey PF, Peres CA (2000) Resource seasonality and the structure of
mixed species bird flocks in a coastal Atlantic forest of southeastern
Brazil. J Trop Ecol 16:33–53
Diehl B (1971) Productivity investigation oftwo types ofmeadows in the
Vistula Valley. XII. Energy requirement in nestling and fledgling
red-backed shrike (Lanius collurio L.). Ekol Pol 19:235–248
Donald PF, Buckingham DL, Moorcroft D, Muirhead LB, Evans AD,
Kirby WB (2001) Habitat use and diet of skylarks Alauda arvensis
wintering on lowland farmland in southern Britain. J Appl Ecol 38:
536–547
Dunham AE (2008) Above and below ground impacts of terrestrial mam-
mals and birds in a tropical forest. Oikos 117:571–579
Dunning JB (2007) CRC handbook of avian body masses, 2nd edn.CRC
Press, Boca Raton
Dyer LA (2002) A quantification of predation rates, indirect positive
effects on plants, and foraging variation of the giant tropical ant
Paraponera clavata. J Insect Sci 2:1–7
Dyrcz A, Flinks H (1995) Nestling and adult diet of the Willie Wagtail
Rhipidura leucophrys near Madang, Papua New Guinea. Emu 95:
123–126
Faanes CA (1982) Avian use of Sheyenne Lake and associated habitats in
central North Dakota. FWS-PUB-144. US Department of Interior,
Fish and Wildlife Service, Washington, DC
Falk JH (1976) Energetics of a suburban lawn ecosystem. Ecology 57:
141–150
Fayt P, Machmer MM, Steeger C (2005) Regulation of spruce bark bee-
tles by woodpeckers—a literature review. Forest Ecol Manag 206:
1–14
Ferger SW, Böhning-Gaese K, Wilcke W, Oelmann Y, Schleuning M
(2013) Distinct carbon sources indicate strong differentiation be-
tween tropical forest and farmland bird communities. Oecologia
171:473–486
Ford HA, BellH (1981) Density of birds in eucalypt woodlandaffected to
varying degrees by dieback. Emu 81:202–208
Fristoe TS (2015) Energy use by migrants and residents in North
American breeding bird communities. Glob Ecol Biogeogr 24:
406–415
GajdošP, Krištín A (1997) Spiders (Araneae) as bird food. In: Zabka M
(ed) Proceedings of the 16
th
European Colloquium of Arachnology,
Siedlce, pp 91–105
Gámez-Virués S, Bonifacio RS, Gurr GM, Kinross C, Raman A, Nicol HI
(2007) Arthropod prey of shelterbelt-associated birds: linking faecal
samples with biological control of agricultural pests. Aust J Entomol
46:325–331
Gaston KJ, Blackburn TM, Goldewijk KK (2003) Habitat conversion and
global avian biodiversity loss. Proc R Soc Lond B Biol Sci 270:
1293–1300
Gibb JA, Betts MM (1963) Food and food supply of nestling tits (Paridae)
in Breckland pine. J Anim Ecol 32:489–533
Gillon D, Adam F, Hubert B, Kahlem G (1983) Production et
consommation de graines en milieu sahélo-soudanien au Sénégal:
bilan général. Rev Ecol (Terre Vie) 38:3–35
Gilroy JJ, Anderson GQ, Grice PV, Vickery JA, Watts PN, Sutherland WJ
(2009) Foraging habitat selection, diet and nestling condition in
Yellow Wagtails Motacilla flava breeding on arable farmland. Bird
Study 56:221–232
Głowaciński Z, Weiner J (1980) Energetics of bird fauna in consecutive
stages of semi-natural pine forest. Ekol Pol 28:71–94
Głowaciński Z, Weiner J (1983) Successional trends in the energetics of
forest bird communities. Ecography 6:305–314
Głowaciński Z, Kozlowski J, Weiner J (1984) Energy and matter flow
through bird populations. In: Grodzinski W, Weiner J, Maycock PF
(eds) Forest ecosystems in industrial regions. Springer, Berlin, pp
125–131
Golley FB (1968) Secondary productivity in terrestrial communities. Am
Zool 8:53–59
Gradwohl J, Greenberg R (1982) The effect of a single species of avian
predator on the arthropods of aerial leaf litter. Ecology 63:581–583
Greenberg R, Bichier P, Angon AC, MacVean C, Perez R, Cano E (2000)
The impact of avian insectivory on arthropods and leaf damage in
some Guatemalan coffee plantations. Ecology 81:1750–1755
Gunnarsson B (1996) Bird predation and vegetation structure affecting
spruce-living arthropods in a temperate forest. J Anim Ecol 65:389–
397
Gutzwiller KJ, Barrow WC (2002) Does bird community structure vary
with landscape patchiness? A Chihuahuan Desert perspective.
Oikos 98:284–298
Hahn S, Bauer S, Liechti F (2009) The natural link between Europe and
Africa—2.1 billion birds on migration. Oikos 118:624–626
Harris RJ (1991) Diet of the wasps Vespula vulgaris and V. germanica in
honeydew beech forest of the South Island, New Zealand. New Zeal
J Zool 18:159–169
Heinrich B, Bell R (1995) Winter food of a small insectivorous bird, the
Golden-crowned Kinglet. Wilson Bull 107:558–561
Helms JA, Godfrey AP, Ames T, Bridge ES (2016) Predator foraging
altitudes reveal the structure of aerial insect communities. Sci Rep
6:28670
Hölldobler B, Wilson EO (1994) Journey to the ants: a story of scientific
exploration. Harvard University Press, Cambridge
Holmes RT (1966) Feeding ecology of the red-backed sandpiper
(Calidris alpina) in Arctic Alaska. Ecology 47:32–45
Holmes RT (1990) Ecological and evolutionary impacts of bird predation
on forest insects: an overview. Stud Avian Biol 13:6–13
Holmes RT, Sturges FW (1973) Annual energy expenditure by the avi-
fauna of a northern hardwoods ecosystem. Oikos 24:24–29
Holmes RT, Sturges FW (1975) Bird community dynamics and energet-
ics in a northern hardwoods ecosystem. J Anim Ecol 44:175–200
Holmes RT, Schultz JC, Nothnagle P (1979) Bird predation on forest
insects: an exclosure experiment. Science 206:462–463
Holmes RT, Sherry TW,Sturges FW (1986) Bird community dynamics in
a temperate deciduous forest: long-term trends at Hubbard Brook.
Ecol Monogr 56:201–220
Hooks CR, Pandey RR, Johnson MW (2003)Impact of avian and arthro-
pod predation on lepidopteran caterpillar densities and plant produc-
tivity in an ephemeral agroecosystem. Ecol Entomol 28:522–532
47 Page 10 of 13 Sci Nat (2018) 105: 47
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Horstmann K (1974) Untersuchungen über den Nahrungserwerb der
Wal damei sen (Formica polyctena Foerster) im Eichenwald.
Oecologia 15:187–204
Howell TR (1971) An ecological study of the birds of the lowland pine
savanna adjacent to rain forest in northeastern Nicaragua. Living
Bird 10:185–242
Humphreys WF (1979) Production and respiration in animal populations.
J Anim Ecol 48:427–453
James FC, Rathbun S (1981) Rarefaction, relative abundance, and diver-
sity of avian communities. Auk 98:785–800
Jenny M (1990) Nahrungsökologie der Feldlerche Alauda arvensis in
einer intensiv genutzten Agrarlandschaft des schweizerischen
Mittellandes. Ornithol Beob 87:31–53
Jeromin K (2002) Zur Ernährungsökologie der Feldlerche (Alauda
arvensis L. 1758) in der Reproduktionsphase. Dissertation.
Universität Kiel, Kiel
Joern A (1986) Experimental study of avian predation on coexisting
grasshopper populations (Orthoptera: Acrididae) in a sandhills
grassland. Oikos 46:243–249
Johnson MD, Kellermann JL, Stercho AM (2010) Pest reduction services
by birds in shade and sun coffee in Jamaica. Anim Conserv 13:140–
147
Kajak A, Breymeyer A, Petal J (1971) Productivity investigation of two
types of meadows in the Vistula Valley. XI. Predatory arthropods.
Ekol Pol A 19:223–233
Kale HW (1965) Ecology and bioenergetics of the long-billed marsh
wren Telmatodytes palustris griseus (Brewster) in Georgia salt
marshes. Publ Nuttall Ornithol Club 5:1–141
Kalka M, Kalko EK (2006) Gleaning bats as underestimated predators of
herbivorous insects: diet of Micronycteris microtis (Phyllostomidae)
in Panama. J Trop Ecol 22:1–10
Karp DS, Mendenhall CD, Sandí RF, Chaumont N, Ehrlich PR, Hadly
EA, Daily GC (2013) Forest bolsters bird abundance, pest control
and coffee yield. Ecol Lett 16:1339–1347
Karr JR (1971) Structure of avian communities in selected Panama and
Illinois habitats. Ecol Monogr 41:207–233
Karr JR (1975) Production, energy pathways, and community diversity in
forest birds. In: Golley EB, Medina E (eds) Tropical ecological
systems: trends in terrestrial and aquatic research. Springer, New
York , p p 1 61–176
Kartanas E (1989) Energy flow through breeding bird communities of
selected environments of the rural landscape. Ekol Pol 37:157–178
Keast A, Recher HF, Ford HA, Saunders DA (1985) Birds of eucalypt
forests and woodlands: ecology, conservation and management.
RAOU and Surrey Beatty, Sydney
Kellermann JL, Johnson MD, Stercho AM, Hackett SC (2008) Ecological
and economic services provided by birds on Jamaican Blue
Mountain coffee farms. Conserv Biol 22:1177–1185
Kelly JF, Bridge ES, Frick WF, Chilson PB (2013) Ecological energetics
of an abundant aerial insectivore, the Purple Martin. PLoS One 8:
e76616
Kennedy CA, Stewart I, Facchini A, Cersosimo I, Mele R, Chen B, Uda
M, Kansal A, Chiu A, Kim KG, Dubeux C, Lebre La Rovere E,
Cunha B, Pincetl S, Keirstead J, Barles S, Pusaka S, Gunawan J,
Adegbile M, Nazariha M, Hoque S, Marcotullio PJ, González
Otharán F, Genena T, Ibrahim N, Farooqui R, Cervantes G, Sahin
AD (2015) Energy and material flows of megacities. Proc Natl Acad
Sci U S A 112:5985–5990
Kirk DA, Evenden MD, Mineau P (1996) Past and current attempts to
evaluate the role of birds as predators of insect pests in temperate
agriculture. Curr Ornithol 13:175–269
Kobal SN, Payne NF, Ludwig DR (1998) Nestling food habits of seven
grassland bird species and insect abundance in grassland habitats in
northern Illinois. Trans Ill State Acad Sci 91:69–75
Koh LP (2008) Birds defend oil palms from herbivorous insects. Ecol
Appl 18:821–825
Korb J, Salewski V (2000) Predation on swarming termites by birds. AfrJ
Ecol 38:173–174
Lasiewski RC, Dawson WR (1967) A re-examination of the relation
between standard metabolic rate and body weight in birds. Condor
69:13–23
Leigh EG (1999) Tropical forest ecology: a view from Barro Colorado
Island. Oxford University Press, New York
Leigh EG, Smythe N (1978) Leaf production, leaf consumption, and the
regulation of folivory on Barro Colorado Island. In: Montgomery
GG (ed) The ecology of arboreal folivores. Smithsonian Institution
Press, Washington, pp 33–50
Lieth H (1973) Primary production: terrestrial ecosystems. Hum Ecol 1:
303–332
Lopes LE, Fernandes AM, Medeiros MC, Marini MÂ (2016) A classifi-
cation scheme for avian diet types. J Field Ornithol 87:309–322
Losey JE, Vaughan M (2006) The economic value of ecological services
provided by insects. Bioscience 56:311–323
Lott CA, Langan BE, Mulrooney MB, Grau RT, Miller KE (2006)
Stopover ecology of nearctic-neotropical migrant songbirds in hard-
wood hammocks of the Florida Keys. Final Report, Florida Fish and
Wildlife Conservation Commission, Tallahassee
Maas B, Tscharntke T, Saleh S, Dwi Putra D, Clough Y (2015) Avian
species identity drives predation success in tropical cacao agrofor-
estry. J Appl Ecol 52:735–743
Maas B, Karp DS, Bumrungsri S, Darras K, Gonthier D, Huang JC,
Lindell CA, Maine JJ, Mestre L, Michel NL, Morrison EB,
Perfecto I, Philpott SM, Şekercioğlu ÇH, Silva RM, Taylor PJ,
Tscharntke T, Van Bael SA, Whelan CJ, Williams-Guillén K
(2016) Bird and bat predation services in tropical forests and agro-
forestry landscapes. Biol Rev 91:1081–1101
Maclean GL (2013) Ecophysiology of desert birds. Springer, Berlin
Mäntylä E, Klemola T, Laaksonen T (2011) Birds help plants: a meta-
analysis of top-down trophic cascades caused by avian predators.
Oecologia 165:143–151
Marone L (1992) Seasonal and year-to-year fluctuations of bird popula-
tions and guilds in the Monte Desert, Argentina (Fluctuaciones
estacionales e interanuales de poblaciones y gremios de aves en el
Desierto del Monte, Argentina). J Field Ornithol 63:294–308
Marquis RJ, Whelan CJ (1994) Insectivorous birds increase growth of
white oak through consumption of leaf-chewing insects. Ecology
75:2007–2014
Michalek KG, Krištín A (2009) Nahrung von Buntspecht Dendrocopos
major Mittelspecht Dendrocopos medius und Baumläufern Certhia
spp. im Wienerwald. Schriftenreihe des Nationalpark Kalkalpen 10:
58–74
Mols CM, Visser ME (2002) Great tits can reduce caterpillar damage in
apple orchards. J Appl Ecol 39:888–899
Montgomerie RD, Cartar RV, McLaughlin RL, Lyon B (1983) Birds of
Sarcpa Lake, Melville Peninsula, Northwest Territories: breeding
phenologies, densities and biogeography. Arctic 36:65–75
Moorman CE, Bowen LT, Kilgo JC, Sorenson CE, Hanula JL, Horn S,
Ulyshen MD (2007) Seasonal diets of insectivorous birds using
canopy gaps in a bottomland forest. J Field Ornithol 78:11–20
Morrison EB, Lindell CA (2012) Birds and bats reduce insect biomass
and leaf damage in tropical forest restoration sites. Ecol Appl 22:
1526–1534
Murakami M, Nakano S (2000) Species-specific bird functions in a
forest-canopy food web. P Roy Soc Lond B Bio 267:1597–1601
Naef-Daenzer L, Naef-Daenzer B, Nager RG (2000) Prey selection and
foraging performance of breeding Great Tits Parus major in relation
to food availability. J Avian Biol 31:206–214
Nilsson SG, Nilsson IN (1976) Numbers, food consumption, and fish
predation by birds in Lake Möckeln, southern Sweden. Ornis
Scand 7:61–70
Sci Nat (2018) 105: 47 Page 11 of 13 47
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Nyffeler M (2000) Ecological impact of spider predation: a critical as-
sessment of Bristowe‘sandTurnbull‘s estimates. Bull Br Arachnol
Soc 11:367–373
Nyffeler M, Birkhofer K (2017) An estimated 400–800 million tons of
prey are annually killed by the global spider community. Sci Nat
104:30
Orłowski G, Karg J, Karg G (2014) Functional invertebrate prey groups
reflect dietary responses to phenology and farming activity and pest
control services in three sympatric species of aerially foraging in-
sectivorous birds. PLoS One 9:e114906
Pagani-Núñez E, Renom M, Mateos-Gonzalez F, Cotín J, Senar JC
(2017) Thediet of great tit nestlings: comparing observation records
and stable isotope analyses. Basic Appl Ecol 18:57–66
Pelikan J (1978) Mammals in the reedswamp ecosystem. In: Dykyjova D,
Kvet J (eds) Pond littoral ecosystems—structure and functioning.
Ecological Studies, vol 28. Springer, Berlin-Heidelberg, pp 357–365
Pelikan J (1993) Consumers in grassland ecosystems at Kamenicky. In:
Rychnovská M (ed) Structure and functioning of seminatural
meadows. Elsevier, Amsterdam, pp 225–243
Perfecto I, Vandermeer JH, Bautista GL, Nunñez GI, Greenberg R,
Bichier P, Langridge S (2004) Greater predation in shaded coffee
farms: the role of resident neotropical birds. Ecology 85:2677–2681
Pershing AJ, Christensen LB, Record NR, Sherwood GD, Stetson PB
(2010) The impact of whaling on the ocean carbon cycle: why big-
ger was better. PLoS One 5:e12444
Pohlert T (2018) PMCMRplus: calculate pairwise multiple comparisons
of mean rank sums extended. R package version 1.0.1. https://
CRAN.R-project.org/package=PMCMRplus (accessed 30 Mar
2018)
Poulin B, Lefebvre G (1996) Dietary relationships of migrant and resident
birds from a humid forest in central Panama. Auk 113:277–287
Poulin B, Lefebvre G, McNeil R (1994) Diets of land birds from north-
eastern Venezuela. Condor 96:354–367
Pravosudov VV, Pravosudova EV (1996) The breeding biology of the
willow tit in northeastern Siberia. Wilson Bull 108:80–93
Ramsay SL, Houston DC (2003) Amino acid composition of some wood-
land arthropods and its implications for breeding tits and other pas-
serines. Ibis 145:227–232
R Core Team (2018) R: a language and environment for statistical com-
puting. R Foundation for Statistical Computing, Vienna, Austria.
URL https://www.R-project.org/ (accessed 30 Mar 2018)
Reagan DP, Waide RB (1996) The food web of a tropical rain forest.
University of Chicago Press, Chicago
Renner SC,Baur S, Possler A, Winkler J, Kalko EK, Bates PJ, Mello MA
(2012) Food preferences of winter bird communities in different
forest types. PLoS One 7:e53121
Robinson MH, Robinson B (1974) A census of web-building spiders in
coffee plantations at Wau, new Guinea, and an assessment of their
insecticidal effects. Trop Ecol 15:95–107
Robinson RA, Sutherland WJ (1997) The feeding ecology of seed-eating
birds on farmland in winter. In: Donald PF, Aebischer NJ (eds) The
ecology and conservation of Corn Buntings Miliaria calandra.UK
Nature Conservation No. 13. Joint Nature Conservation Committee,
Peterborough, pp 162–169
Robinson WD, Brawn JD, Robinson SK (2000) Forest bird community
structure in central Panama: influence of spatial scale and biogeog-
raphy. Ecol Monogr 70:209–235
Roslin T, Hardwick B, Novotny V, Petry WK, Andrew NR, Asmus A,
Barrio IC, Basset Y, Boesing AL, Bonebrake TC, Cameron EK
(2017) Higher predation risk for insect prey at low latitudes and
elevations. Science 356:742–744
Rotenberry JT (1980a) Dietary relationships among shrubsteppe passer-
ine birds: competition or opportunism in a variable environment.
Ecol Monogr 50:93–110
Rotenberry JT (1980b) Bioenergetics and diet in a simple community of
shrubsteppe birds. Oecologia 46:7–12
Sakai S (2002) General flowering in lowland mixed dipterocarp forests of
South-East Asia. Biol J Linn Soc 75:233–247
Sam K, Koane B, Jeppy S, Sykorova J, Novotny V (2017) Diet of land
birds along an elevational gradient in Papua New Guinea. Sci Rep 7:
44018
Sanderson MG (1996) Biomass of termites and their emissions of meth-
ane and carbon dioxide: a global database. Global Biogeochem Cy
10:543–557
Saugier B, Roy J, Mooney HA (2001) Estimations of global terrestrial
productivity: converging toward a single number? In: Roy J, Saugier
B, Mooney HA (eds) Terrestrial global productivity. Academic
Press, San Diego, pp 543–557
Scebba S (2001) Biometrics and sex ratios of skylarks Alauda arvensis
during migration in southern Italy. Ringing Migr 20:364–370
Schaefer M (1990) The soil fauna of a beech forest on limestone: trophic
structure and energy budget. Oecologia 82:128–136
Schaub M, Jenni L (2000) Fuel deposition of three passerine bird species
along the migration route. Oecologia 122:306–317
Şekercioğlu CH (2006a) Ecological significance of bird populations.
Handbook of the birds of the world 11:15-51. Lynx Edicions,
Barcelona http://www.hbw.com/ (accessed 16 June 2017)
Şekercioğlu CH (2006b) Increasing awareness of avian ecological func-
tion. Trends Ecol Evol 21:464–471
Şekercioğlu ÇH, Ehrlich PR, Daily GC,Aygen D, Goehring D, Sandí RF
(2002) Disappearance of insectivorous birds from tropical forest
fragments. Proc Natl Acad Sci U S A 99:263–267
Şekercioğlu ÇH, Daily GC, Ehrlich PR (2004) Ecosystem consequences
of bird declines. Proc Natl Acad Sci U S A 101:18042–18047
Şekercioğlu ÇH, Wenny D, Whelan CJ (eds) (2016) Why birds matter.
University of Chicago Press, Chicago
Shelly TE (1986) Rates of prey consumption by neotropical robber flies
(Diptera: Asilidae). Biotropica 18:166–170
Shorthouse DJ, Marples T (1982) The life stages and population dynam-
icsofanaridzonescorpionUrodacus yaschenkoi (Birula, 1903).
Aust J Ecol 7:109–118
Shvarts EA, Chernyshev NV, Popov IY (1997)Do shrews have an impact
on soil invertebrates in Eurasian forests? Ecoscience 4:158–162
Smith KG, MacMahon JA (1981) Bird communities along a montane
sere: community structure and energetics. Auk 98:8–28
Sokolov V, Ehrich D, Yoccoz NG, Sokolov A, Lecomte N (2012) Bird
communities of the Arctic shrub tundra of Yamal: habitat specialists
and generalists. PLoS One 7:e50335
Solonen T (1986) Stability of a bird community in southern Finland.
Ornis Scand 17:106–116
Stewart MM, Woolbright LL (1996) Amphibians. In: Reagan DP, Waide
RB (eds) The food web of a tropical rain forest. University of
Chicago Press, Chicago, pp 273–320
Strong AM, Sherry TW, Holmes RT (2000) Bird predation on herbivo-
rous insects: indirect effects on sugar maple saplings. Oecologia
125:370–379
Suthers HB, Bickal JM, Rodewald PG (2000) Use of successional habitat
and fruit resources by songbirds during autumn migration in central
New Jersey. Wilson Bull 112:249–260
Szaro RC, Balda RP (1979) Bird community dynamics in a ponderosa
pine forest. Stud Avian Biol 3:1–66
Terborgh J (1989) Where have all the birds gone? Princeton University
Press, Princeton
Terborgh J, Robinson SK, Parker TA, Munn CA, Pierpont N (1990)
Structure and organization of an Amazonian forest bird community.
Ecol Monogr 60:213–238
Tima TB (1957) Die jahreszeitlichen Änderungen der
Nahrungsbeziehungen der Vögel und der primären Schädlinge der
Kiefer in Latvian SSR. Waldhygiene 2:93–194
Török J, Tóth L (1999) Asymmetric competition between two tit species:
a reciprocal removal experiment. J Anim Ecol 68:338–345
47 Page 12 of 13 Sci Nat (2018) 105: 47
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Tremblay I, Thomas D, Blondel J, Perret P, Lambrechts MM (2005) The
effect of habitat quality on foraging patterns, provisioning rate and
nestling growth in Corsican blue tits Parus caeruleus. Ibis 147:17–
24
Tscharntke T, Şekercioğlu ÇH, Dietsch TV, Sodhi NS, Hoehn P,
Tylianakis JM (2008) Landscape constraints on functional diversity
of birds and insects in tropical agroecosystems. Ecology 89:944–
951
Tuttle MD (1994) The lives of Mexican free-tailed bats. Bats 12:6–14
UNESCO (1979) Tropical grazing land ecosystems: a state-of-knowledge
report. UNESCO, Paris
Uramoto M (1961) Ecological study of the bird community of the broad-
leaved deciduous forest of central Japan. J Yamashina Inst Ornithol
3(1):1–32
Van Bael SA, Brawn JD, Robinson SK (2003) Birds defend trees from
herbivores in a neotropical forest canopy. Proc Natl Acad Sci U S A
100:8304–8307
Vel’ký M, Kanuch P, Krištín A (2011) Food composition of wintering
great tits (Parus major): habitat and seasonal aspects. Folia Zool 60:
228–236
Walter H, Breckle SW (2013) Ecological systems of the geobiosphere: II.
Tropical and subtropical zonobiomes. Springer, Berlin-Heidelberg
Watson A (1963) Bird numbers on tundra in Baffin Island. Arctic 16:101–
108
Weathers WW (1983) Birds of Southern California’s Deep Canyon.
University of California Press, Berkeley
Wei ner J, Głowaciński Z (1975) Energy flow through a bird community
in a deciduous forest in southern Poland. Condor 77:233–242
Wenny DG, Devault TL, Johnson MD, Kelly D, Şekercioğlu CH,
Tomback DF, Whelan CJ (2011) The need to quantify ecosystem
services provided by birds. Auk 128:1–14
West GC, DeWolfe BB (1974) Populations and energetics of taiga birds
near Fairbanks, Alaska. Auk 91:757–775
Whelan CJ, Wenny DG, Marquis RJ (2008) Ecosystem services provided
by birds. Ann N Y Acad Sci 1134:25–60
Whelan CJ, Şekercioğlu ÇH, Wenny DG (2015) Why birds matter: from
economic ornithology to ecosystem services. J Ornithol 156:227–
238
Wielgolaski FE (1975) Productivity of tundra ecosystems. In: Reichle
DE, Franklin JF, Goodall DW (eds) Proceedings of a symposium
on productivity of world ecosystems. National Academy of
Sciences, Washington, DC, pp 1–12
Wiens JA(1973) Pattern and process in grassland bird communities. Ecol
Monogr 43:237–270
Wiens JA (1977) Model estimation of energy flow in North American
grassland bird communities. Oecologia 31:135–151
Wiens JA (1989) The ecology of bird communities, Vol. 1. Cambridge
University Press, Cambridge, UK
Wiens JA (1991) Ecological similarity of shrub-desert avifaunas of
Australia and North America. Ecology 72:479–495
Wiens JA, Dyer MI (1975) Simulation modelling of red-winged black-
bird impact on grain crops. J Appl Ecol 12:63–82
Wiens JA, Nussbaum RA (1975) Model estimation of energy flow in
northwestern coniferous forest bird communities. Ecology 56:547–
561
Wikelski M, Tarlow EM, Raim A, Diehl RH, Larkin RP, Visser GH
(2003) Avian metabolism: costs of migration in free-flying song-
birds. Nature 423:704–704
Williams JB, Batzli GO (1979) Winter diet of a bark-foraging guild of
birds. Wilson Bull 91:126–131
Willson MF (1974) Avian community organization and habitat structure.
Ecology 55:1017–1029
Wilson JD, Morris AJ, Arroyo BE, Clark SC, Bradbury RB (1999) A
review of the abundance and diversity of invertebrate and plant
foods of granivorous birds in northern Europe in relation to agricul-
tural change. Agric Ecosyst Environ 75:13–30
Woronecki PP, Dolbeer RA (1980) The influence of insects in bird dam-
age control. In: Clark JP (ed) Proceedings 9
th
vertebrate pest control
conference. University of California, Davis, pp 53–59
Zandt HS (1997) Water content of prey of nestling blue tits in a Corsican
habitat. Neth J Zool 47:125–131
Sci Nat (2018) 105: 47 Page 13 of 13 47
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

1.
2.
3.
4.
5.
6.
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers and authorised users (“Users”), for small-
scale personal, non-commercial use provided that all copyright, trade and service marks and other proprietary notices are maintained. By
accessing, sharing, receiving or otherwise using the Springer Nature journal content you agree to these terms of use (“Terms”). For these
purposes, Springer Nature considers academic use (by researchers and students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and conditions, a relevant site licence or a personal
subscription. These Terms will prevail over any conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription
(to the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of the Creative Commons license used will
apply.
We collect and use personal data to provide access to the Springer Nature journal content. We may also use these personal data internally within
ResearchGate and Springer Nature and as agreed share it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not
otherwise disclose your personal data outside the ResearchGate or the Springer Nature group of companies unless we have your permission as
detailed in the Privacy Policy.
While Users may use the Springer Nature journal content for small scale, personal non-commercial use, it is important to note that Users may
not:
use such content for the purpose of providing other users with access on a regular or large scale basis or as a means to circumvent access
control;
use such content where to do so would be considered a criminal or statutory offence in any jurisdiction, or gives rise to civil liability, or is
otherwise unlawful;
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association unless explicitly agreed to by Springer Nature in
writing;
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a systematic database of Springer Nature journal
content.
In line with the restriction against commercial use, Springer Nature does not permit the creation of a product or service that creates revenue,
royalties, rent or income from our content or its inclusion as part of a paid for service or for other commercial gain. Springer Nature journal
content cannot be used for inter-library loans and librarians may not upload Springer Nature journal content on a large scale into their, or any
other, institutional repository.
These terms of use are reviewed regularly and may be amended at any time. Springer Nature is not obligated to publish any information or
content on this website and may remove it or features or functionality at our sole discretion, at any time with or without notice. Springer Nature
may revoke this licence to you at any time and remove access to any copies of the Springer Nature journal content which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or guarantees to Users, either express or implied
with respect to the Springer nature journal content and all parties disclaim and waive any implied warranties or warranties imposed by law,
including merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published by Springer Nature that may be licensed
from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a regular basis or in any other manner not
expressly permitted by these Terms, please contact Springer Nature at
onlineservice@springernature.com