Biological Control 56 (2011) 107–114

Contents lists available at ScienceDirect

Biological Control
journal homepage: www.elsevier.com/locate/ybcon

Review

Birds as predators of the pine processionary moth (Lepidoptera: Notodontidae)

Luc Barbaro a,⇑, Andrea Battisti b
a
INRA, UMR1202 Biodiversity, Genes and Communities, 69 route d’Arcachon, F-33612 Cestas, France
b
Department of Environmental Agronomy and Crop Production, University of Padova, Viale dell’Università, Legnaro, Padova, Italy

a r t i c l e i n f o a b s t r a c t

Article history: The beneficial role of insectivorous birds potentially contributing to the biological control of forest insect
Received 4 May 2010 pests appears crucial in the context of climate warming, especially for species currently expanding their
Accepted 23 October 2010 range such as the pine processionary moth Thaumetopoea pityocampa. Larvae of T. pityocampa are apose-
Available online 29 October 2010
matic and carry true urticating setae which, together with overwintering in silk winter nests, prevent
them from predation by most insectivorous forest birds. The present review aims at pointing out which
Keywords: bird species can regularly feed on this key forest defoliator throughout its distribution range, and which
Avian predation
predation strategies allow birds to cope with the urticating setae carried by late-instar larvae. At least
Biological control
Insect defoliator
seven bird species can be considered as regular predators of the pine processionary moth: four large
Pine forests migrant specialists (great spotted cuckoo Clamator glandarius, common cuckoo Cuculus canorus, European
Thaumetopoea pityocampa nightjar Caprimulgus europaeus and Eurasian hoopoe Upupa epops) and three small sedentary generalists
Urticating setae (great tit Parus major, crested tit Lophophanes cristatus and coal tit Periparus ater). Each species has devel-
oped morphological traits and foraging techniques to feed on different life stages of T. pityocampa
throughout the year: (i) gizzard wall structure allowing the consumption of caterpillars with urticating
setae (cuckoos); (ii) nocturnal foraging on moth imagos by aerial hawking (nightjars); (iii) ground prob-
ing on below-ground pupae with long curved bill (hoopoe); and (iv) shifted predation period in autumn
and winter on eggs, early- and late-instar larvae, with particular feeding technique allowing to eat only
the inner parts of urticating larvae stages (tits). Although several avian predators regularly feed on T.
pityocampa, only a few specialist and generalist insectivorous birds may contribute to regulate its popu-
lations, especially when population density of the moth is low. Moreover, their efficiency may possibly be
threatened by mismatches associated with climate change.
Ó 2010 Elsevier Inc. All rights reserved.

1. Introduction Insectivorous birds have proven to be very efficient predators,

Insectivorous birds are increasingly acknowledged as poten-
tially efficient agents contributing to the biological control of agri-
cultural and forest insect pests worldwide (Hooks et al., 2003; Fayt
et al., 2005; Ji et al., 2008; Van Bael et al., 2008). Bird communities
consequently provide ecosystem services that may be of high eco-
nomic value (Mols and Visser, 2002; Koh, 2008; Whelan et al.,
2008), especially in the context of climate warming, which is
expected to increase distribution ranges and outbreaks of insect
pests in the future (Netherer and Schopf, 2009; Thomson et al.,
2010). The impact of bird predation on insect pests, however, is
likely to be noticeable only in non-outbreak conditions, i.e., when
insect pest populations are low (Crawford and Jennings, 1989;
Holmes, 1990; Glen, 2004). Climate change is also assumed to
modify community interactions and consequently the relative
importance of generalist and specialist predators of herbivorous in-
sects (Gilman et al., 2010).
⇑ Corresponding author. Fax: +33 5 57122881.
E-mail address: luc.barbaro@pierroton.inra.fr (L. Barbaro).
able to reduce by 20% to 100% the populations of forest pest
Lepidoptera which they feed on (Crawford and Jennings, 1989;
Whelan et al., 1989; Cooper and Smith, 1995; Parry et al., 1997;
Tanhuanpää et al., 2001; Mols and Visser, 2002; Hooks et al.,
2003). Lepidoptera larvae are actually the main prey for a large
number of European forest insectivorous birds and especially tits
(Paridae), for which they represent up to 70% of the diet (Kristin
and Patocka, 1997). Although all life stages can be depredated,
including imagos, birds generally prefer large and glabrous cater-
pillars and 95% of Lepidoptera are consumed at the late-instar lar-
val stages (Whelan et al., 1989; Kristin and Patocka, 1997; Parry
et al., 1997; Tanhuanpää et al., 2001). High rates of avian predation
are generally considered to contribute maintaining Lepidoptera
populations at low densities (Holmes, 1990; Glen, 2004). However,
no effect of bird predation is detected above a density of 106 cater-
pillars/ha, i.e., during outbreaks (Crawford and Jennings, 1989).
Insectivorous birds often exhibit numerical and functional re-
sponses to moth fluctuations (Crawford and Jennings, 1989; Patten
and Burger, 1998; Jones et al., 2003; Hogstad, 2005). They can
aggregate where prey density is higher, although generally at

1049-9644/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved.
doi:10.1016/j.biocontrol.2010.10.009
108 L. Barbaro, A. Battisti / Biological Control 56 (2011) 107–114
spatial scales larger than a tree (Diaz et al., 1998; Fayt et al., 2005;
Barber et al., 2008; Norris and Martin, 2008). Dietarily specialized
species (sensu Sherry, 1990) such as cuckoos (Cuculidae) are able
to respond to spatio-temporal fluctuations of aposematic Lepidop-
tera such as Lymantria dispar or Malacosoma spp. by gathering in
outbreak areas during their post-migratory nomadic phase (Payne,
1997; Hoyas and López, 1998; Gale et al., 2001; Barber et al., 2008).
However, the overall effect of cuckoo predation in controlling the
outbreaks of, i.e., Malacosoma spp. is likely to be negligible, even
if a single cuckoo is able to remove hundred of caterpillars during
a few days (Payne, 1997). Such a clumped pattern of foraging birds
in areas with high food availability is also found in generalist insec-
tivorous passerines such as tits (Diaz et al., 1998; Forsman et al.,
2009). Tits can actually concentrate on food resources locally, for
example in areas of Thaumetopoea pityocampa outbreaks (Pimentel
and Nilsson, 2007).
The pine processionary moth T. pityocampa is currently showing
an expansion northwards and higher in altitude in Europe due to
increased winter temperatures (Hodar and Zamora, 2004; Battisti
et al., 2005; Robinet et al., 2007). As a defoliator, it can cause severe
damage to forests, but because larvae can release urticating setae,
it is also a serious threat to humans and domestic mammals. Its
natural enemies are numerous and include avian predators (Battis-
ti et al., 2000), although the urticating setae seem to be a strong
deterrent (Battisti et al., 2011). Moreover, T. pityocampa larvae bury
into the soil in late winter for pupation, which allows them to es-
cape a period of intense predation in spring, during avian breeding
season (Crawford and Jennings, 1989; Holmes, 1990). An outbreak
of T. pityocampa may therefore have an overall negative effect on
forest bird communities by reducing other palatable insects
through severe defoliation (Gale et al., 2001). However, a recent
study did not demonstrate such a negative effect (Pimentel and
Nilsson, 2009), as already observed during gypsy moth outbreaks
(Bell and Whitmore, 2000; Gale et al., 2001; Showalter and Whit-
more, 2002). Avian predation on the pine processionary moth has
been documented for a long time, but no up-to-date synthesis
has ever been attempted, and many information has never been
published in English (e.g., Gil-Lletget, 1945; Biliotti, 1958; Valver-
de, 1971; Gonzalez Cano, 1981; Battisti, 1986; Hoyas and López,
1998; Barbaro et al., 2003).
The aim of the present review is therefore to document: (i) the
mechanisms involved in the predation of hairy Lepidoptera larvae
by birds, and especially the strategies used for avoiding the inges-
tion of urticating setae; (ii) the bird species that can be considered
as regular predators of the pine processionary moth throughout its
distribution range, and their likely response to climate change; and
(iii) the stages of moth life cycle consumed, the predation periods
and the foraging techniques used by predatory birds.
2. Strategies of bird predation on hairy Lepidoptera
Aposematic and hairy Lepidoptera larvae such as the pine pro-
cessionary moth are often considered to be relatively immune to
avian attack (Kristin and Patocka, 1997; Parry et al., 1997; Glen,
2004; Marples and Roper, 2004). However, there is increasing evi-
dence that hairy Lepidoptera larvae including Malacosoma disstria,
Lymantria dispar, Dendrolimus punctatus or Nyctemera annulata may
be highly affected by bird predation in natural conditions, even
when glabrous caterpillars are available as alternative preys (Gill,
1980; Whelan et al., 1989; Wang and Liao, 1990; Parry et al.,
1997; Veldtman et al., 2007; Barber et al., 2008). In particular,
avian predation on the gypsy moth L. dispar has been extensively
studied and birds were responsible of variable but significant pre-
dation of moth egg masses (up to 71% of predation rate, Higashiura,
1989; up to 53%, Cooper and Smith, 1995).
Some insectivorous birds have actually developed particular
strategies to cope with larvae covered by urticating setae, with dif-
ferent level of specialization among species (Table 1). Dietary spe-
cialization is defined as a restricted niche breadth for feeding
requirements, i.e., a narrow range of resources used by a given spe-
cies, leading to dietary homogeneity and particular foraging behav-
iors (Sherry, 1990; Devictor et al., 2010; Terraube et al., 2010).
Birds that have evolved strategies to feed on aposematic and toxic
insects are actually considered as dietarily specialized (Sherry,
1990). One of these feeding strategies is to rupture caterpillars
by banging them on branches to discard the head capsule and
the integument, and eat only the viscera (Gill, 1980; Payne,
1997). This behavior is used by cuckoos (Cuculidae) worldwide,
but also by several species of forest passerines such as northern
oriole Icterus galbula, least flycatcher Empidonax minimus or yellow
warbler Dendroica petechia in North America (Parry et al., 1997),
and tits (Paridae) in Europe (Gonzalez Cano, 1981; Halperin, 1990).
Cuckoos and hoopoes (Upupidae) are also able to clean larvae
from their setae by rubbing them on the ground (Payne, 1997;
Kristin, 2001), but the best adaptation to feed on hairy caterpillars
is found on several cuckoo species of at least the genera Cuculus,
Chrysococcyx, Clamator or Coccyzus (Table 1). In these species, the
gizzard inner layer has evolved towards a soft, thick and non-ker-
atinoid structure that allows the larvae setae to be kept inserted in
the gizzard wall and to be regurgitated as mixed pellets of mucous
membrane and setae (Gill, 1980). A long and curved bill structure
also allows hoopoes Upupa epops to dig out buried pupae from be-
low-ground, and together with rollers Coracias spp., hornbills Tock-
us spp. or northern orioles I. galbula, they can also break rigid
cocoons to extract pupae by continuously rubbing them on the
ground (Parry et al., 1997; Battisti et al., 2000; Kristin, 2001; Veldt-
man et al., 2007). In addition, urticating Lepidoptera can also be
consumed at non-toxic life stages such as eggs, early-instar larvae
or imagos (Table 1), although in some species adult moths are also
carrying urticating setae (e.g., Euproctis spp. in Europe, and many
others in Africa and South America).
3. Birds as predators of the pine processionary moth
The pine processionary moth is the most severe defoliator of
pine forests in south-western Europe, North Africa and the Near
East (Battisti et al., 2000). Its populations are included in three
main clades, two of which correspond to two species: T. pityocam-
pa from north-western Africa to eastern Turkey, T. wilkinsoni from
eastern Turkey to Israel, and a third distinct clade in central-north
and north-eastern Africa (Kerdelhue et al., 2009). Larvae of T. pityo-
campa feed by night on pine needles from autumn to spring and
they develop silk nests at the top of pine tree canopies (especially
Pinus nigra, P. sylvestris, P. halepensis, P. brutia, P. pinea and P. pinas-
ter) where they can resist cold temperatures during the winter
(Battisti et al., 2005). At the end of the winter they execute proces-
sions and bury into the first centimeters of the soil before pupa-
tion; then adult moths emerge from the ground during the
following summer to oviposit their egg-batches (Battisti et al.,
2000; Hodar and Zamora, 2004). Only a few species of insectivo-
rous birds have developed adaptations to feed on T. pityocampa,
which shows traits apparently protecting from bird predation:
eggs are covered with scales by the female, larvae are hidden in
winter nests during the day and covered with urticating setae at
the late-instar stages, and pupae are buried into the soil (Halperin,
1990; Battisti et al., 2000).
At least seven species of insectivorous birds have been cited as
regular predators of the pine processionary moth throughout its
range: four large non-passerine migrants with a specialist diet,
and three small resident passerines with a more generalist diet
 L. Barbaro, A. Battisti / Biological Control 56 (2011) 107–114 109

Table 1
Classification of predation strategies used by insectivorous birds to feed on hairy Lepidoptera larvae, with decreasing level of specialization among species.

Predation strategy Specialization Bird species involved Main sources

1. Soft gizzard wall structure allowing to
regurgitate urticating setae
2. Long curved bill structure used to dig
out buried pupae
3. Discarding urticating integument of
larvae
4. Breaking pupae cocoons with the bill
5. Shifted predation on non-urticating
stages (moths, eggs, early-instar
larvae)
High Cuckoos (at least of genera Cuculus, Chrysococcyx, Meise and Schifter (1972), Gill (1980), Payne
Clamator, Coccyzus) (1997)
High Hoopoes (Upupidae) Battisti et al. (2000), Barbaro et al. (2008)
Moderate Cuckoos, tits (Paridae), North-American passerines Gill (1980), Gonzalez Cano (1981), Halperin
(Icterus galbula, Empidonax minimus, Dendroica petechia) (1990), Parry et al. (1997), Payne (1997)
Moderate Hoopoes, rollers Coracias spp., hornbills Tockus spp., Parry et al. (1997), Battisti et al. (2000),
northern oriole Icterus galbula Kristin (2001), Veldtman et al. (2007)
Low Nightjars (Caprimulgidae), tits and probably other forest Gonzalez Cano (1981), Cleere (1999), Sierro
passerines et al. (2001), Pimentel and Nilsson (2007)

(Table 2). Moreover, at least four species can exhibit numerical or
functional responses to the moth density at different life stages
(Table 2). Among large specialist species, the two species of Euro-
pean cuckoos (great spotted cuckoo Clamator glandarius and com-
mon cuckoo Cuculus canorus) have a specialized diet on late-instar
Lepidoptera larvae, and especially urticating species such as T.
pityocampa, which they consume during pre-pupation processions
in spring (Gil-Lletget, 1945; Valverde, 1953; Meise and Schifter,
1972; Khoptynskii, 1976; Payne, 1997; Hoyas and López, 1998).
The Eurasian hoopoe U. epops is also able to specialize on T. pityo-
campa pupae while breeding in spring and early summer (Battisti
et al., 2000; Barbaro et al., 2008). The European nightjar Caprimul-
gus europaeus has a specialized diet dominated by adult moths in
summer (Auclair, 1988; Cleere, 1999; Sierro et al., 2001) and is
likely to feed locally on T. pityocampa during summer emergence,
as observed repeatedly in south-western France (Barbaro et al.,
2003).
Among small generalist passerines, the great tit Parus major is
able to consume late-instar larvae, eggs or imagos of T. pityocampa
and to aggregate locally during periodic outbreaks (Gonzalez Cano,
1981; Halperin, 1990; Pimentel and Nilsson, 2007, 2009). Two
other tit species occurring in pine forests (the crested tit Lopho-
phanes cristatus and the coal tit Periparus ater) are also able to feed
on eggs and early-instar larvae, at least in late summer and early
autumn (Gonzalez Cano, 1981). We therefore suggest that the ef-
fect of predation by these different species may be complementary
in time and space because of distinct foraging methods and periods
(Philpott et al., 2009), allowing a temporal succession of predation
covering the complete life cycle of the prey: eggs, early- and late-
instar larvae (within winter nests or during processions), pupae,
and imagos.
4. Cuckoos’ strategy: consuming urticating larvae
Two European species of cuckoos are highly adapted to feed on
urticating caterpillars thanks to their soft gizzard wall structure
(Gill, 1980; Nakamura and Miyazawa, 1997; Payne, 1997). The
great spotted cuckoo C. glandarius is a large insectivorous bird dis-
tributed throughout the Mediterranean region, with a specialized
diet on gregarious hairy caterpillars such as T. pityocampa, Ocnogy-
na baetica (Arctiidae) or Chondrostega vandalicia (Lasiocampidae) in
central Spain (Gil-Lletget, 1945; Valverde, 1953; Soler et al., 1994;
Payne, 1997; Hoyas and López, 1998). The common cuckoo C. can-
orus, more widely distributed and less dietary specialized than the
former species, is also considered a specialist predator of hairy cat-
erpillars (Gil-Lletget, 1945; Ishizawa and Chiba, 1966; Khoptynskii,
1976; Nakamura and Miyazawa, 1997; Payne, 1997), and espe-
cially of T. pityocampa larvae in Europe (Biliotti, 1958; Meise and
Schifter, 1972; Jarry, 1994). Adults of these trans-Saharan migrants
get back early from their African wintering grounds, typically in
late February or early March, when the late-instar larvae (L4 and
L5) of the pine processionary moth are available as an abundant
food resource (Table 2). Caterpillars are typically depredated with-
in the winter nests or on the ground when they execute their pre-
pupation processions by following chemical trails (Halperin, 1990;
Hoyas and López, 1998).
Adult great spotted cuckoos have a very specialized diet during
the breeding season, with 100% of the birds feeding on T. pityocam-
pa in central Spain in March–April (22–41 caterpillars per stomach,
mean = 32.8, n = 11) (Valverde, 1953). In southern Spain, 42% of
males offered Lepidoptera larvae to their females against 17% each
for Coleoptera and Orthoptera (Soler, 1990). By contrast, juvenile
great spotted cuckoos are not able to feed on T. pityocampa larvae

Table 2
Bird species regularly feeding on the pine processionary moth Thaumetopoea pityocampa (PPM) in Europe, North Africa and the Near East. Predation periods are indicated by
months (II = February, III = March, IV = April, V = May, VI = June, VII = July, VIII = August, IX = September, X = October).

Bird species Body size Predated moth Predation Foraging technique Numerical and/or functional Main sources
(cm) stages period response
Large specialists
Clamator 35–39 Mature larvae II–IV Ground and canopy Yes (100% of stomachs Valverde (1971), Hoyas and López (1998)
glandarius gleaning contained PPM)
Cuculus 32–34 Mature larvae III–IV Ground and canopy Likely (Lepidoptera larvae are Gill (1980), Gonzalez Cano (1981)
canorus gleaning 75% of diet)
Caprimulgus 24–28 Moths VII–VIII Aerial hawking or Likely (moths are 80–90% of Sierro et al. (2001), Barbaro et al. (2003)
europaeus flycatching diet)
Upupa epops 26–32 Pupae, mature III–VI Ground probing and Yes (70% of PPM pupae Battisti et al. (2000), Barbaro et al. (2008)
larvae gleaning predated)
Small generalists
Parus major 14 Eggs, larvae, IX–V Canopy and ground Yes (60–90% of stomachs Gonzalez Cano (1981), Pimentel and
moths gleaning contained PPM) Nilsson (2007, 2009)
Lophophanes 11.5 Eggs, larvae IX–IV Canopy and ground Likely Gonzalez Cano (1981)
cristatus gleaning
Periparus ater 11.5 Eggs, larvae X–IV Canopy gleaning Yes (60% of stomachs Gonzalez Cano (1981)
contained PPM)
110 L. Barbaro, A. Battisti / Biological Control 56 (2011) 107–114
when they leave the nests and still depend for 25–59 days on their
magpie hosts (Pica pica) to be fed on beetles and grasshoppers that
they are unable to catch by themselves (Soler et al., 1994). As a re-
sult, the specialization of cuckoos on hairy caterpillars is probably
acquired later, when the bird is adult or sub-adult (Gill, 1980). In
southern Europe, habitat selection by C. glandarius is both deter-
mined by pine processionary moth density and by the presence
of its obligate host, the magpie (Valverde, 1971; Soler, 1990; Hoyas
and López, 1998). Great spotted cuckoos are highly territorial and
defend large territories covering up to 3.7 km2 (Arias-de-Reyna
et al., 1987). The selection of habitats with high food resource
availability is probably achieved during their post-migratory no-
madic phase, i.e., the time period just after returning from winter-
ing grounds, as observed in Coccyzus cuckoos (Gale et al., 2001;
Barber et al., 2008).
C. canorus has been repeatedly observed consuming T. pityocam-
pa larvae after spring arrival in Pinus nigra forests of northern Italy,
and larvae were taken mainly from processions both on trees and
on the ground. A captive young cuckoo male has been fed with T.
pityocampa larvae during no-choice assays, and was observed
regurgitating pellets after their ingestion, which were irregularly
shaped and contained pine needle fragments (larval gut content)
mixed with hairs, urticating setae, and insect integument frag-
ments (Battisti, unpubl.). Common cuckoos are actually known to
eject the undigestible part of the larvae with the pellet, including
the urticating setae (Meise and Schifter, 1972; Gill, 1980). In Japan,
results of diet analyses have shown that Lepidoptera larvae consti-
tuted 75% of prey in 82 cuckoo stomachs (Ishizawa and Chiba,
1966). A male common cuckoo has been observed foraging on
the ground and catching 32 hairy caterpillars in ca 2 h, i.e., one
every 4 min (Nakamura and Miyazawa, 1997). Cuckoos never sing
or call within their foraging areas in order to avoid attacks from
host bird species, so that breeding and foraging areas are com-
pletely distinct (Nakamura and Miyazawa, 1997). Feeding areas
are large, covering 24 ha on average for males and 28 ha for fe-
males respectively; they are typically distant of 2–3 km for females
and more than 4 km for males from their breeding areas (Nakam-
ura and Miyazawa, 1997; Payne, 1997). Foraging common cuckoos
favor short herbaceous vegetation such as grazed pastures despite
lower arthropod abundance, suggesting that higher food accessi-
bility in short vegetation is more important than overall prey
abundance (Romanowski and Zmihorski, 2008).
5. Nightjars’ strategy: nocturnal feeding on adult moths
The European nightjar C. europaeus is a large trans-Saharan mi-
grant and insectivorous specialist able to catch adult moths by aer-
ial hawking at dusk and at dawn, and by flycatching later in the
night (Alexander and Cresswell, 1990; Cleere, 1999). Nightjars fre-
quently use roads and forest tracks at night as observation plat-
forms to detect moth silhouettes against twilight skies (Jackson,
2003). Nocturnal imagos of Lepidoptera are one of the most impor-
tant preys for nightjars, representing, e.g., 35% of the stomachs
studied in afro-tropical species (Jackson, 2000) or 41% of the diet
for the common nighthawk Chordeiles minor (Todd et al., 1998).
The European nightjar has a very specialized diet, with 81–93%
of the prey biomass composed of moths (Sierro et al., 2001) and
up to 13 moths were found in one male’s gizzard feeding its young
(Auclair, 1988). Nightjars are likely to be very efficient predators
able to catch up to 18–19 prey items per minute and to capture
more than one insect at a time, as shown for C. minor (Todd
et al., 1998; Cleere, 1999).
Foraging C. europaeus favor open habitats such as clearings and
forest edges for hunting moths and flying insects (Cleere, 1999).
They avoid dense pine forests that are unsuitable for aerial hawk-
ing, even if prey abundance is higher within than outside pine for-
ests (Sierro et al., 2001). European nightjars are favoured by mosaic
landscapes including several habitats such as deciduous and pine
forests, open habitats or wetlands, and they can fly up to 10–
15 km to feed in areas with abundant preys (Alexander and Cres-
swell, 1990; Sierro et al., 2001; Barbaro et al., 2007). C. europaeus
is potentially an important predator of T. pityocampa in pine forests
of southern Europe (Gonzalez Cano, 1981). European nightjars can
reach a relatively high density in pine plantations of south-western
France (ca 1 pair/30 ha), where they have been regularly observed
between mid-July and early August feeding on adult pine proces-
sionary moths when they fly around pheromone traps (Barbaro
et al., 2003). In the Swedish island of Götland, C. europaeus is also
a likely predator of the northern pine processionary moth Thau-
metopoea pinivora, as it has been repeatedly observed to fly around
the emergence sites of the moth during the flight period of imagos.
Moreover, another nightjar species occurs within T. pityocampa
distribution range, the red-necked nightjar C. ruficollis, which is
also a predator of adult moths and moth larvae (Cleere, 1999).
The red-necked nightjar inhabits pine woodlands in southern Spain
and can locally reach higher breeding densities (1.2–4 nests/10 ha)
than C. europaeus (Cuadrado and Dominguez, 1996).
6. Hoopoes’ strategy: ground probing on buried pupae
The Eurasian hoopoe U. epops is another large insectivorous spe-
cialist using a typical ground probing technique to forage on large
below-ground arthropods with their long curved bill (5–6 cm)
(Kristin, 2001). This trans-Saharan migrant arrives in southern Eur-
ope in late February or early March, when pre-pupation proces-
sions of T. pityocampa occur, and leaves in August and September
(Reichlin et al., 2009). As a specialist ground prober, foraging hoop-
oes select particular micro-habitats with short sward structure
such as mown borders of track edges or grazed pastures for easy
access to buried preys (Fournier and Arlettaz, 2001; Barbaro
et al., 2008; Romanowski and Zmihorski, 2008). The Eurasian hoo-
poe is considered as an important predator of T. pityocampa and
other agricultural and forest pest insects in several countries
including Spain, France, Italy, Switzerland, Israel or China (Gonz-
alez Cano, 1981; Halperin, 1990; Wang and Liao, 1990; Battisti
et al., 2000; Fournier and Arlettaz, 2001; Kristin, 2001). Orthoptera
and Coleoptera are generally its main preys, although Hymenop-
tera and Lepidoptera also represent significant parts of the diet
(Kristin and Patocka, 1997). Lepidoptera larvae and pupae repre-
sent up to 67% in frequency of hoopoe diet in Switzerland and
29% of biomass supplied to the chicks, even if molecrickets Gry-
llotalpa gryllotalpa are energetically more advantageous, represent-
ing 26% in frequency and 68% of biomass (Fournier and Arlettaz,
2001).
In pine plantation forests of southern Europe (Italy, France),
hoopoes specialize on T. pityocampa larvae and especially on be-
low-ground pupae (Battisti et al., 2000; Barbaro et al., 2008). Pupae
are present all year long because their diapause can extend over
several years, making them available immediately after hoopoe
spring arrival, but also after moth emergence during summer. In Pi-
nus nigra plantation forests of northern Italy, up to 68–74% of pu-
pae can be consumed by hoopoes, contributing strongly to
population regulation under non-outbreak conditions (Battisti
et al., 2000). In Pinus pinaster plantations of south-western France,
breeding hoopoes significantly select pine stand edges with short
herbaceous vegetation (<7 cm) along forest tracks as foraging mi-
cro-habitats within mean home ranges of 13 ha (Barbaro et al.,
2008). Foraging areas hence closely match with micro-habitats
used by T. pityocampa for below-ground pupation, and depredated
cocoons are left on the ground by hoopoes after pulling out the pu-
 L. Barbaro, A. Battisti / Biological Control 56 (2011) 107–114
pae (Battisti et al., 2000). Winter nest density of T. pityocampa in
pine stand edges was also positively correlated with hoopoe forag-
ing intensity and nesting success during three consecutive years,
pointing out a density-dependent relationships during non-out-
break conditions (Barbaro et al., 2008).
7. Tits’ strategy: removing urticating setae from larvae
The great tit Parus major is a small sedentary passerine with a
widespread distribution range in Europe. Although a generalist
predator throughout the year, it has a relatively specialized diet
during the breeding season, mainly feeding its chicks with larvae
of Lepidoptera, especially geometrids and tortricids (Naef-Daenzer
and Keller, 1999; Mols and Visser, 2002). Great tits are ‘inflexible
perch-gleaners’ concentrating on trees with the highest available
biomass and always selecting the larger preys (Diaz et al., 1998;
Hino et al., 2002). They have been reported to feed upon egg clus-
ters, early-instar or late-instar larvae of T. pityocampa in several
Mediterranean countries including Israel (Halperin, 1990), France
(Biliotti, 1958), Spain (Gonzalez Cano, 1981) or Portugal (Pimentel
and Nilsson, 2009). The most efficient predation period occurs in
February–March (Table 2), when great tits make holes into T. pityo-
campa winter nests in order to collect late-instar larvae. They re-
move the head capsule and most of the integument carrying
urticating setae to eat only inner parts of the larval body (Gonzalez
Cano, 1981; Halperin, 1990). In Spain, diet analyses revealed that
up to 60–90% of stomachs and excrements contained T. pityocampa
larvae (Gonzalez Cano, 1981). The great tit can also feed on adult
moths (Barba et al., 1994), including adults of T. pityocampa from
populations showing a delayed phenology with adult moths avail-
able during tits’ breeding season (Pimentel and Nilsson, 2007). For-
aging great tits are therefore able to aggregate during summer in
areas with local outbreaks of T. pityocampa populations (Pimentel
and Nilsson, 2009).
Together with the great tit, other Paridae species are able to
cluster in areas with the highest food availability throughout the
year in European forests (Diaz et al., 1998). They thus provide reli-
able cues for indicating habitat quality to other forest birds such as
stop-over migrants (Forsman et al., 2009). Crested tit L. cristatus
and coal tit Periparus ater have a more restricted range than P. ma-
jor since they are generally restricted to conifer forests (Blondel,
1985; Maicas and Fernandez Haeger, 2004). The crested tit usually
forages in pine canopies in summer, whereas it prefers tree
branches and trunk, or the ground in winter (Diaz et al., 1998).
The coal tit is a generalist forager feeding on small preys in trees
with low food availability (Blondel, 1985; Hino et al., 2002). It
has a less specialized diet than other tits, with 28% of Lepidoptera
(Kristin and Patocka, 1997), and favors edges for foraging in winter
because of higher pine seed availability (Brotons and Herrando,
2003). Coal and crested tits mainly feed on T. pityocampa eggs
and non-urticating early-instar larvae, and they can also use holes
made by great tits in winter nests (Gonzalez Cano, 1981). In central
Spain, the coal tit can also extract viscera of late-instar larvae with
urticating setae, and up to 66% of P. ater stomachs and excrements
contained pine processionary moth, with peak predation periods in
October–December and April–May (Gonzalez Cano, 1981).
Blue tit Cyanistes caeruleus and long-tailed tit Aegithalos cauda-
tus are highly gregarious outside the breeding season and have also
been reported as at least occasional predators of T. pityocampa eggs
and early-instar larvae until L3-stage in autumn and winter (Gonz-
alez Cano, 1981). Other bird species reported as only occasional
predators of the pine processionary moth in Europe include turdids
(blackbird Turdus merula, rock thrush Monticola saxatilis) and cor-
vids (chough Pyrrhocorax pyrrhocorax, carrion crow Corvus corone)
(Gonzalez Cano, 1981). In addition, long-tailed tits and several frin-
111
gillids (goldfinch Carduelis carduelis, chaffinch Fringilla coelebs, and
European serin Serinus serinus) can actively collect the silken
threads from T. pityocampa larval nests to build their own nests,
possibly causing additional larval mortality in early spring (Halper-
in, 1990).
8. Discussion: specialist vs generalist predators of T. pityocampa
The present review suggests that only a small number of spe-
cialist and generalist insectivorous birds may contribute to main-
tain T. pityocampa populations at low abundance levels within its
distribution range. A density-dependent bird predation must actu-
ally be sustained through time and space to efficiently control Le-
pidopteran pests by maintaining low population densities, but this
seems only possible under non-outbreak conditions (Crawford and
Jennings, 1989; Holmes, 1990; Glen, 2004). Thus, the question
arises if bird predation on the pine processionary moth can really
contribute to control abundance levels of this key forest defoliator.
Large insectivorous birds with a specialized diet on caterpillars and
moths such as cuckoos, hoopoes or nightjars have either a narrow
distribution range in Europe (C. glandarius) or generally occur at
low densities in most European pine forests (U. epops, C. europaeus).
To date, only predation by the Eurasian hoopoe has been proven to
be important enough on T. pityocampa pupae to play a significant
role for controlling local populations (Battisti et al., 2000). The
most specialized predatory bird of the pine processionary moth
is the great spotted cuckoo, but its real efficiency on controlling
populations is virtually unknown although the bird shows a strong
numerical response to its prey (Hoyas and López, 1998). Studies on
North-American Coccyzus cuckoos have shown that their predation
on hairy caterpillars was unlikely to have a significant effect in
controlling the prey populations, and despite cuckoos can elimi-
nate entire colonies of Malacosoma larvae (Payne, 1997).
Generalist predators can be effective biocontrol agents
(Symondson et al., 2002) and a significant positive response of
two generalist passerines (P. major and T. merula) to T. pityocampa
outbreaks has been recently demonstrated (Pimentel and Nilsson,
2009). The generalist predation hypothesis predicts that a predator
community dominated by generalists may stabilize prey popula-
tions at low abundance levels, although generalists show weaker
numerical responses to prey fluctuations than specialists (Dupuy
et al., 2009; Terraube et al., 2010). Such a higher role of generalists
than specialists on stabilizing pest populations can be explained by
a temporary specialization by generalists switching their diet from
alternative preys during pest outbreaks (Dupuy et al., 2009),
although it is not necessary always the case for outbreaking Lepi-
doptera. Concerning the predatory bird guild of T. pityocampa, we
suggest that high functional complementarity occur between the
bird species involved, able to feed on all life stages of the moth
and hence likely to have a significant overall impact on prey re-
moval (Philpott et al., 2009). If predation by specialists on pine pro-
cessionary moth is higher in spring due to their breeding
phenology (Hoyas and López, 1998; Battisti et al., 2000), general-
ists such as P. major can feed on others stages from summer to win-
ter, even in ‘summer’ moth populations having a shifted phenology
(Pimentel and Nilsson, 2009), due to their high adaptive plasticity
(Charmantier et al., 2008). However, generalists are more likely to
consume large hairy larvae when these are aggregated because of
increased handling time compared to smaller, glabrous ones (Parry
et al., 1997). In addition, the impact of avian predators on parasit-
oids of T. pityocampa may be negative or neutral, depending on
parasitoid life-history traits (Battisti et al., 2000; Tanhuanpää
et al., 2001; Glen, 2004). For example, tachinid parasitoids are
more severely affected by bird predation than hymenopteran par-
asitoids, since tachinids and birds use the same cues to locate their
112 L. Barbaro, A. Battisti / Biological Control 56 (2011) 107–114
host or prey, but not hymenopterans that are thus able to limit the
risk of bird predation (Veldtman et al., 2007).
The response of generalist and specialist bird predators of T.
pityocampa to climate change is also a challenging question. In
the range expansion area, mortality is generally low and only gen-
eralist birds such as tits have been shown to feed on the colonies in
autumn and spring (Battisti et al., 2005; Buffo et al., 2007). Tits are
known to respond to climate change through phenological shifts
that are tracking those of the prey (Charmantier et al., 2008; Bauer
et al., 2010), although in the case of the pine processionary moth
the synchrony does not seem to be as important as in oak-feeding
Lepidoptera. The distribution of breeding birds along an altitudinal
gradient in the Alps showed a shift of about 29 m per decade (Popy
et al., 2010), that is less than half of that observed for T. pityocampa
in similar conditions (70 m per decade, see Battisti et al., 2005),
implying a possible mismatch between the insect and its preda-
tors. We should thus expect that the expansion areas are character-
ized by a reduced bird predation, caused mainly by generalist
species.
9. Conclusion and management implications
Bird predation on T. pityocampa may be favoured through the
provision of artificial nestboxes to enhance local population of cav-
ity-nesting predators, and by adequate stand- and landscape-scale
management of pine forests. Among specialist predatory birds,
only U. epops can be actually favoured by providing specific nest-
boxes (Fournier and Arlettaz, 2001; Barbaro et al., 2008). The low
density of breeding cavities in pine plantations with short silvicul-
tural rotations is a limiting factor for populations of cavity-nesting
birds, including hoopoe and tits (Maicas and Fernandez Haeger,
2004; Pimentel and Nilsson, 2007). The great tit is the main gener-
alist predatory bird able to seasonally consume T. pityocampa lar-
vae, and for which nestboxes can be used to increase local
populations (Wang and Liao, 1990; Mols and Visser, 2002; Bouvier
et al., 2005).
The accessibility of T. pityocampa to predatory birds also de-
pends on adequate management of pine forest stands and their
edges, as demonstrated for C. europaeus and U. epops, and varies
according to moth life stages and bird foraging techniques (Battisti
et al., 2000; Sierro et al., 2001). Prey accessibility is more important
than overall prey abundance to determine the intensity of bird pre-
dation, according to the distinct foraging strategies used by the dif-
ferent bird species (Sierro et al., 2001; Romanowski and Zmihorski,
2008). For example, herbaceous edges of pine stands along forest
tracks are the preferred micro-habitats for below-ground pupation
because of positive phototaxis of pupating larvae, and they match
narrowly with the preferential foraging micro-habitats for hoopoes
and cuckoos (Battisti et al., 2000; Barbaro et al., 2008; Romanowski
and Zmihorski, 2008). Because of higher food abundance or acces-
sibility, pine stand edges are also important foraging micro-habi-
tats for nightjars (Cleere, 1999) or coal tits in winter (Brotons
and Herrando, 2003).
The pine processionary moth is the subject of extensive control
all over the Mediterranean basin, with about 2,50,000 ha sprayed
annually with Bacillus thuringiensis kurstaki and insect growth reg-
ulators. This control could have a potential impact on avian preda-
tors by reducing prey availability and seasonal productivity of
insectivorous birds (Gale et al., 2001; Marshall et al., 2002; Glen,
2004). An indirect effect could also be identified in the concurrent
reduction of non-target Lepidoptera (Marshall et al., 2002),
although few species are active during the spray period against T.
pityocampa. The conservation biological control of the pine proces-
sionary moth through the maintenance of diverse habitat mosaics
favorable to a diversity of natural enemies, including insectivorous
birds, should therefore be considered at the landscape scale
(Tscharntke et al., 2007; Eilers and Klein, 2009). Fragments of na-
tive deciduous forest have a functional role in landscapes domi-
nated by homogeneous pine plantations by providing
complementary resources to insectivorous birds (Gonzalez-Gomez
et al., 2006; Barbaro et al., 2007), but also to other vertebrate (e.g.,
bats) or invertebrate (e.g., Calosoma sycophanta, Ephippiger ephippi-
ger) predators of this key insect pest. As recently underlined by
Thomson et al. (2010), climate warming may also result in a future
mismatch between shifted populations of T. pityocampa and its
specialist avian predators, in both space and time.
Acknowledgments
We warmly acknowledge all the people that have provided
information for this review, namely B. Barthelemy, A.M. Dulaurent,
B. Giffard, F. Goussard, F. Jean, J.C. Martin, P. Menassieu, J. Nezan, D.
Piou, A. Roques, J. Rousselet and F. Vetillard. We are also indebted
to F. Archaux, T. Boivin, J.C. Bouvier, J.A. Hodar, H. Jactel, S. Larsson
and I. van Halder, who helped improving the earlier versions of the
manuscript. This work was funded by French National Research
Agency in the framework of project ANR n°07BDIV 013
‘URTICLIM’..
References
Alexander, I., Cresswell, B., 1990. Foraging by nightjars Caprimulgus europaeus away
from their nesting areas. Ibis 132, 568–574.
Arias-de-Reyna, L., Recuerda, P., Trujillo, J., Corvillo, M., Cruz, A., 1987. Territory in
the great spotted cuckoo (Clamator glandarius). Journal of Ornithology 128,
231–239.
Auclair, R., 1988. Synthèse d’une étude sur l’engoulevent d’Europe (Caprimulgus
europaeus) en Allier. Le Grand-Duc 38, 1–34.
Barba, E., García, D.M., Gil-Delgado, J.A., López, G.M., 1994. Moth abundance and
breeding success in a Great Tit population where moths are the main nestling
food. Ardea 82, 329–334.
Barbaro, L., Nezan, J., Bakker, M., Revers, F., Couzi, L., Vetillard, F., Le Gall, O., 2003.
Distribution par habitats des oiseaux nicheurs à enjeu de conservation en forêt
des Landes de Gascogne. Le Courbageot 21–22, 12–23.
Barbaro, L., Rossi, J.P., Vetillard, F., Nezan, J., Jactel, H., 2007. The spatial distribution
of birds and carabid beetles in pine plantation forests: the role of landscape
composition and structure. Journal of Biogeography 34, 652–664.
Barbaro, L., Couzi, L., Bretagnolle, V., Nezan, J., Vetillard, F., 2008. Multi-scale habitat
selection and foraging ecology of the eurasian hoopoe (Upupa epops) in pine
plantations. Biodiversity and Conservation 17, 1073–1087.
Barber, N.A., Marquis, R.J., Tori, W.P., 2008. Invasive prey impacts regional
distribution of native predators. Ecology 89, 2678–2683.
Battisti, A., 1986. Osservazioni sull’attivita predatoria dell’upupa Upupa epops a
carico della processionaria del pino Thaumetopoea pityocampa. Avocetta 10,
119–121.
Battisti, A., Bernardi, M., Ghiraldo, C., 2000. Predation by the hoopoe on pupae of
Thaumetopoea pityocampa and the likely influence on other natural enemies.
Biocontrol 45, 311–323.
Battisti, A., Stastny, M., Netherer, S., Robinet, C., Schopf, A., Roques, A., Larsson, S.,
2005. Expansion of geographic range in the pine processionary moth caused by
increased winter temperatures. Ecology 15, 2084–2096.
Battisti, A., Holm, G., Fagrell, B., Larsson, S., 2011. Urticating hairs in arthropods:
their nature and medical significance. Annual Review of Entomology 56, 203–
220.
Bauer, Z., Trnka, M., Bauerová, J., Možný, M., Štěpánek, P., Bartošová, L., Žalud, Z.,
2010. Changing climate and the phenological response of great tit and collared
flycatcher populations in floodplain forest ecosystems in Central Europe.
International Journal of Biometeorology 54, 99–111.
Bell, J.L., Whitmore, R.C., 2000. Bird nesting ecology in a forest defoliated by gypsy
moths. Wilson Bulletin 112, 524–531.
Biliotti, E., 1958. Les parasites et prédateurs de Thaumetopoea pityocampa Schiff.
(Lepidoptera). Entomophaga 3, 23–24.
Blondel, J., 1985. Breeding strategies of the blue tit and coal tit (Parus) in mainland
and island Mediterranean habitats: a comparison. Journal of Animal Ecology 54,
531–556.
Bouvier, J.C., Toubon, J.F., Boivin, T., Sauphanor, B., 2005. Effects of apple orchard
management strategies on the great tit (Parus major) in southeastern France.
Environmental Toxicology and Chemistry 24, 2846–2852.
Brotons, L., Herrando, S., 2003. Effect of increased food abundance near forest edges
on flocking patterns of Coal Tit Parus ater winter groups in mountain coniferous
forests. Bird Study 50, 106–111.
 L. Barbaro, A. Battisti / Biological Control 56 (2011) 107–114
Buffo, E., Battisti, A., Stastny, M., Larsson, S., 2007. Temperature as a predictor of
survival of the pine processionary moth in the Italian Alps. Agricultural and
Forest Entomology 9, 65–72.
Charmantier, A., McCleery, R.H., Cole, L.R., Perrins, C., Kruuk, L.E.B., Sheldon, B.C.,
2008. Adaptive phenotypic plasticity in response to climate change in a wild
bird population. Science 320, 800–803.
Cleere, N., 1999. Family caprimulgidae (Nightjars). In: del Hoyo, J., Elliott, A.,
Sargatal, J. (Eds.), Handbook of the Birds of the World, Barn-owls to
Hummingbirds, vol. 5. Lynx Edicions, Barcelona, pp. 302–386.
Cooper, R.J., Smith, H.R., 1995. Predation on gypsy moth (Lepidoptera:
Lymantriidae) egg masses by birds. Environmental Entomology 24, 571–575.
Crawford, H.S., Jennings, D.T., 1989. Predation by birds on spruce budworm
Choristoneura fumiferana: functional, numerical, and total responses. Ecology
70, 152–163.
Cuadrado, M., Dominguez, F., 1996. Phenology and breeding success of Red-necked
Nightjar Caprimulgus ruficollis in Southern Spain. Journal für Ornithologie 137,
249–253.
Devictor, V., Clavel, J., Julliard, R., Lavergne, S., Mouillot, D., Thuiller, W., Venail, P.,
Villeger, S., Mouquet, N., 2010. Defining and measuring ecological
specialization. Journal of Applied Ecology 47, 15–25.
Diaz, M., Illera, J.C., Atienza, J.C., 1998. Food resource matching by foraging tits Parus
spp. during spring–summer in a Mediterranean mixed forest: evidence for an
ideal free distribution. Ibis 140, 654–660.
Dupuy, G., Giraudoux, P., Delattre, P., 2009. Numerical and dietary responses of a
predator community in a temperate zone of Europe. Ecography 32, 277–290.
Eilers, E.J., Klein, A.M., 2009. Landscape context and management effects on an
important insect pest and its natural enemies in almond. Biological Control 51,
388–394.
Fayt, P., Machmer, M.M., Steeger, C., 2005. Regulation of spruce bark beetles by
woodpeckers: a literature review. Forest Ecology and Management 206, 1–14.
Forsman, J.T., Hjernquist, M.B., Gustafsson, L., 2009. Experimental evidence for the
use of density based interspecific social information in forest birds. Ecography
32, 539–545.
Fournier, J., Arlettaz, R., 2001. Food provision to nestlings in the Hoopoe Upupa
epops: implications for the conservation of a small endangered population in
the Swiss Alps. Ibis 143, 2–10.
Gale, G.A., DeCecco, J.A., Marshall, M.R., McClain, W.R., Cooper, R.J., 2001. Effects of
gypsy moth defoliation on forest birds: an assessment using breeding bird
census data. Journal of Field Ornithology 72, 291–304.
Gil-Lletget, A., 1945. Bases para un estudio científico de alimentación en las aves y
resultado del análisis de 400 estómagos. Boletín de la Real Sociedad Española de
Historia Natural 43, 9–23.
Gill, B.J., 1980. Foods of the shining cuckoo (Chrysococcyx lucidus, Aves: Cuculidae)
in New Zealand. New Zealand Journal of Ecology 3, 138–140.
Gilman, S.E., Urban, M.C., Tewksbury, J., Gilchrist, G.W., Holt, R.D., 2010. A
framework for community interactions under climate change. Trends in
Ecology and Evolution 25, 325–331.
Glen, D.M., 2004. Birds as predators of lepidopterous larvae. In: van Hemden, H.,
Rothschild, M. (Eds.), Insect and Bird Interactions. Intercept, Andover, pp. 89–
106.
Gonzalez Cano, J.M., 1981. Predacion de procesionaria del pino por vertebrados en
la zona de Mora de Rubielos (Teruel). Boletin de la Estacion Central de Ecologia
10, 53–77.
Gonzalez-Gomez, P.L., Estades, C.F., Simonetti, J.A., 2006. Strengthened insectivory
in a temperate fragmented forest. Oecologia 148, 137–143.
Halperin, J., 1990. Natural enemies of Thaumetopoea spp. (Lep., Thaumetopoeidae)
in Israel. Journal of Applied Entomology 109, 425–435.
Higashiura, Y., 1989. Survival of eggs in the gypsy moth Lymantria dispar. I.
Predation by birds. Journal of Animal Ecology 58, 403–412.
Hino, T., Unno, A., Nakano, S., 2002. Prey distribution and foraging preference for
tits. Ornithological Science 1, 81–87.
Hodar, J.A., Zamora, R., 2004. Herbivory and climatic warming: a Mediterranean
outbreaking caterpillar attacks a relict, boreal pine species. Biodiversity and
Conservation 13, 493–500.
Hogstad, O., 2005. Numerical and functional responses of breeding passerine
species to mass occurrence of geometrid caterpillars in a subalpine birch forest:
a 30-year study. Ibis 147, 77–91.
Holmes, R.T., 1990. Ecological and evolutionary impacts of bird predation on forest
insects: an overview. Studies in Avian Biology 13, 6–13.
Hooks, C.R.R., Pandey, R.R., Johnson, M.W., 2003. Impact of avian and arthropod
predation on lepidopteran caterpillar densities and plant productivity in an
ephemeral agroecosystem. Ecological Entomology 28, 522–532.
Hoyas, J., López, F., 1998. Distribución del críalo según la abundancia de
procesionaria del pino. Quercus 149, 20–22.
Ishizawa, J., Chiba, S., 1966. Food analysis of four species of cuckoos in Japan.
Miscellaneous Reports of the Yamashina Institute for Ornithology 4, 302–326.
Jackson, H.D., 2000. The food of the Afrotropical nightjars. Ostrich 71, 408–415.
Jackson, H.D., 2003. A field survey to investigate why nightjars frequent roads at
night. Ostrich 74, 97–101.
Jarry, G., 1994. Coucou gris Cuculus canorus. In: Yeatman-Berthelot, D., Jarry, G.
(Eds.), Nouvel atlas des oiseaux nicheurs de France. Société Ornithologique de
France, Paris, pp. 386–387.
Ji, R., Simpson, S.J., Yua, F., He, Q.X., Yun, C.J., 2008. Diets of migratory rosy starlings
(Passeriformes: Sturnidae) and their effects on grasshoppers: implications for a
biological agent for insect pests. Biological Control 46, 547–551.
113
Jones, J., Doran, P.J., Holmes, R.T., 2003. Climate and food synchronize regional forest
bird abundances. Ecology 84, 3024–3032.
Kerdelhue, C., Zane, L., Simonato, M., Salvato, P., Rousselet, J., Roques, A., Battisti, A.,
2009. Quaternary history and contemporary patterns in a currently expanding
species. BMC Evolutionary Biology 9, 220.
Khoptynskii, V.I., 1976. The cuckoo, an enemy of hairy caterpillars. Zashchita
Rastenii 8, 62.
Koh, L.P., 2008. Birds defend oil palms from herbivorous insects. Ecological
Applications 18, 821–825.
Kristin, A., 2001. Family upupidae (Hoopoe). In: del Hoyo, J., Elliott, A., Sargatal, J.
(Eds.), Handbook of the Birds of the World, Mousebirds to Hornbills, vol. 6. Lynx
Edicions, Barcelona, pp. 396–411.
Kristin, A., Patocka, J., 1997. Birds as predators of Lepidoptera: selected examples.
Biologia 52, 319–326.
Maicas, R., Fernandez Haeger, J., 2004. Pine plantations as a breeding habitat for a
hole-nesting bird species crested tit (Parus cristatus) in southern Spain. Forest
Ecology and Management 195, 267–278.
Marples, N.M., Roper, T.J., 2004. Warning colours and warning smells: how birds
learn to avoid aposematic insects. In: van Hemden, H., Rothschild, M. (Eds.),
Insect and Bird Interactions. Intercept, Andover, pp. 185–192.
Marshall, M.R., Cooper, R.J., DeCecco, J.A., Strazanac, J., Butler, L., 2002. Effects of
experimentally reduced prey abundance on the breeding ecology of the red-
eyed vireo. Ecological Applications 12, 261–280.
Meise, W., Schifter, H., 1972. The cuckoos and their relatives. In: Grzimek, B. (Ed.),
Grzimek’s Animal Life Encyclopedia, vol. 8. Van Nostrand Reinhold, New York.
Mols, C.M.M., Visser, M.E., 2002. Great tits can reduce caterpillar damage in apple
orchards. Journal of Applied Ecology 39, 888–899.
Naef-Daenzer, B., Keller, L.F., 1999. The foraging performance of great and blue tits
(Parus major and P. Caeruleus) in relation to caterpillar development, and its
consequences for nestling growth and fledging weight. Journal of Animal
Ecology 68, 708–718.
Nakamura, H., Miyazawa, Y., 1997. Movements, space use and social organisation of
radio-tracked common cuckoos during the breeding season in Japan. Japanese
Journal of Ornithology 46, 23–54.
Netherer, S., Schopf, A., 2009. Potential effects of climate change on insect
herbivores in European forests – general aspects and the pine processionary
moth as specific example. Forest Ecology and Management 259, 831–838.
Norris, A.R., Martin, K., 2008. Mountain pine beetle presence affects nest patch
choice of red-breasted nuthatches. Journal of Wildlife Management 72, 733–
737.
Parry, D., Spence, J.R., Volney, W.J.A., 1997. Responses of natural enemies to
experimentally increased populations of the forest tent caterpillar, Malacosoma
disstria. Ecological Entomology 22, 97–108.
Patten, M.A., Burger, J.C., 1998. Spruce budworm outbreaks and the incidence of
vagrancy in eastern North American wood-warblers. Canadian Journal of
Zoology 76, 433–439.
Payne, R.B., 1997. Family Cuculidae (Cuckoos). In: del Hoyo, J., Elliott, A., Sargatal, J.
(Eds.), Handbook of the Birds of the World, Sandgrouses to Cuckoos, vol. 4. Lynx
Edicions, Barcelona, pp. 508–607.
Philpott, S.M., Soong, O., Lowenstein, J.H., Pulido, A.L., Lopez, D.T., Flynn, D.F.B.,
DeCleck, F., 2009. Functional richness and ecosystem services: bird predation on
arthropods in tropical agroecosystems. Ecological Applications 19, 1858–1867.
Pimentel, C., Nilsson, J.A., 2007. Response of great tits Parus major to an irruption of
a pine processionary moth Thaumetopoea pityocampa population with a shifted
phenology. Ardea 95, 191–199.
Pimentel, C., Nilsson, J.A., 2009. Response of passerine birds to an irruption of a pine
processionary moth Thaumetopoea pityocampa population with a shifted
phenology. Ardeola 56, 189–203.
Popy, S., Bordignon, L., Prodon, R., 2010. A weak upward elevational shift in the
distributions of breeding birds in the Italian Alps. Journal of Biogeography 37,
57–67.
Reichlin, T.S., Schaub, M., Menz, M.H.M., Mermod, M., Portner, P., Arlettaz, R., Jenni,
L., 2009. Migration patterns of Hoopoe Upupa epops and Wryneck Jynx torquilla:
an analysis of European ring recoveries. Journal of Ornithology 150, 393–400.
Robinet, C., Baier, P., Pennerstorfer, J., Schopf, A., Roques, A., 2007. Modelling the
effects of climate change on the potential feeding activity of Thaumetopoea
pityocampa (Den. & Schiff.) (Lep., Notodontidae) in France. Global Ecology and
Biogeography 16, 460–471.
Romanowski, J., Zmihorski, M., 2008. Selection of foraging habitat by grassland
birds: effect of prey abundance or availability? Polish Journal of Ecology 56,
365–370.
Sherry, T.W., 1990. When are birds dietarily specialized? Distinguishing ecological
from evolutionary approaches. Studies in Avian Biology 13, 337–352.
Showalter, C.R., Whitmore, R.C., 2002. The effect of gypsy moth defoliation on
cavity-nesting bird communities. Forest Science 48, 273–281.
Sierro, A., Arlettaz, R., Naef-Daenzer, B., Strebel, S., Zbinden, N., 2001. Habitat use
and foraging ecology of the nightjar Caprimulgus europaeus in the Swiss Alps:
towards a conservation scheme. Biological Conservation 98, 325–331.
Soler, M., 1990. Relationships between the great spotted cuckoo Clamator glandarius
and its magpie hosts in a recently colonized area. Ornis Scandinavica 21, 212–
223.
Soler, M., Palomino, J.J., Martinez, J.G., Soler, J.J., 1994. Activity, survival,
independence and migration of fledgling great spotted cuckoos. Condor 96,
802–805.
114 L. Barbaro, A. Battisti / Biological Control 56 (2011) 107–114
Symondson, W.O.C., Sunderland, K.D., Greenstone, M.H., 2002. Can generalist
predators be effective biocontrol agents? Annual Review of Entomology 47,
561–594.
Tanhuanpää, M., Ruohomaki, K., Uusipaikka, E., 2001. High larval predation rate in
non-outbreaking populations of a geometrid moth. Ecology 82, 281–289.
Terraube, J., Arroyo, B., Madders, M., Mougeot, F., 2010. Diet specialisation and
foraging efficiency under fluctuating vole abundance: a comparison between
generalist and specialist avian predators. Oikos, doi:10.1111/j.1600-
0706.2010.18554.x.
Thomson, L.J., Macfadyen, S., Hoffmann, A.A., 2010. Predicting the effects of
climate change on natural enemies of agricultural pests. Biological Control 52,
296–306.
Todd, L.D., Poulin, R.G., Brigham, R.M., 1998. Diet of common nighthawks (Chordeiles
minor: Caprimulgidae) relative to prey abundance. American Midland
Naturalist 139, 20–28.
Tscharntke, T., Bommarco, R., Clough, Y., Crist, T.O., Kleijn, D., Rand, T.A., Tylianakis,
J.A., van Nouhuys, S., Vidal, S., 2007. Conservation biological control and enemy
diversity on a landscape scale. Biological control 43, 294–309.
Valverde, J.A., 1953. Contribution a la biologie du coucou geai, Clamator glandarius L.
I. Notes sur le coucou-geai en Castille. L’Oiseau et R.F.O 23, 288–296.
Valverde, J.A., 1971. Notas sobre la biologia reproductora del crialo Clamator
glandarius (L.). Ardeola, numero especial, 591–647.
Van Bael, S.A., Philpott, S.M., Greenberg, R., Bichier, P., Barber, N.A., Mooney, K.A.,
Gruner, D.S., 2008. Birds as predators in tropical agroforestry systems. Ecology
89, 928–934.
Veldtman, R., Mc Geoch, M.A., Scholtz, C.H., 2007. Can life-history and defence traits
predict the population dynamics and natural enemy responses of insect
herbivores? Ecological Entomology 32, 662–673.
Wang, Y.H., Liao, Y.J., 1990. Attracting beneficial birds for the biological control of
Dendrolimus punctatus (Lep. Lasiocampidae). Chinese Journal of Biological
Control 6, 25–26.
Whelan, C.J., Holmes, R.T., Smith, H.R., 1989. Bird predation on gypsy moth
(Lepidoptera: Lymantriidae) larvae: an aviary study. Environmental
Entomology 18, 43–45.
Whelan, C.J., Wenny, D.G., Marquis, R.J., 2008. Ecosystem services provided by birds.
Annals of the New York Academy of Sciences 1134, 25–60.