Response of Passerine Birds to an Irruption of a Pine Processionary Moth Thaumetopoea Pityocampa Population with a Shifted Phenology

Ardeola 56(2), 2009, 189-203

RESPONSE OF PASSERINE BIRDS TO AN IRRUPTION OF A PINE PROCESSIONARY MOTH THAUMETOPOEA PITYOCAMPA POPULATION WITH A SHIFTED PHENOLOGY

RESPUESTA DE LAS PASERIFORMES A LA IRRUPCIÓN DE LA PROCESIONARIA DEL PINO THAUMETOPOEA PITYOCAMPA CON FENOLOGÍA VARIADA

Carla PIMENTEL* 1 and Jan-Åke NILSSON**

SUMMARY.—Response of passerine birds to an irruption of a pine processionary moth Thaumetopoea pityocampa population with a shifted phenology. The main purpose of the present work was to investigate if the passerine community was able to respond to a localized irruption of a temporally shifted population of the pine processionary moth Thaumetopoea pityocampa, the larval development of which takes place during the summer, called summer population (SP). The work was conducted in the National Pine Forest of Leiria, a highly organised production forest, essentially consisting of maritime pine, Pinus pinaster, and located in the central west coast of Portugal (39º 50` N, 8º 57` W, 30 - 50 m a.s.l.). The SP irrupted in a homogeneous area consisting of young pines. Bird abundances and richness were estimated by point counts in the infested area and in two similar non-infested areas. The counts were made during all four seasons, covering all stages of the moth annual cycle and were repeated during two years. The overall abundance of birds was similar in both infested and non-infested areas. However, the richness of canopy gleaners was higher in the SP area than in a nearby non-infested area. Only two bird species responded numerically to the increased insect abundance: the blackbird Turdus merula, and the great tit Parus major. Thus the passerine community responded only to a limited degree to the irruption of the SP. Three factors might have accounted for the results: (i) the bird community consists mostly of territorial residents or short distance migrants and their low range of dispersal may decrease the probability of a response to a localized insect outbreak. (ii) The larvae of the pine processionary moth has urticating hairs which are considered to be an effective repellent defence against vertebrate predators, thus reducing the number of species that could react to the high caterpillar densities. (iii) The simple vegetation structure of the forest, homogeneous stands of small young trees, precludes the establishment of cavity nesters that constitute a large part of the canopy gleaners and most of the species which have been reported as potential T. pityocampa predators. However, results indicate that this important Mediterranean defoliator may have a positive effect on the canopy gleaners and on some species that are able to act as its predators. Key words: bird community, insect defoliator, insect outbreak, life-cycle shift, Mediterranean pine forest, numerical response, point count.

* DCEA/FCT, Universidade Nova de Lisboa. PT-2825-516 Campus de Caparica, Portugal. ** Department of Animal Ecology, Lund University. S-223 62 Lund, Sweden.

1 Corresponding author: [email protected] 190 PIMENTEL, C. and NILSSON, J. Å.

RESUMEN.—Respuesta de las paseriformes a la irrupción de la procesionaria del pino Thaumetopo- ea pityocampa con fenología variada. El propósito principal de este trabajo fue investigar si la comunidad de paseriformes respondería a una irrupción local de la procesionaria del pino Thaumetopea pityocampa en una población con cambios temporales, cuyo desarrollo de larvas ocurre en verano (llamada población de verano, PV). El trabajo se desarrolló en el Bosque Nacional de Pino de Leiria (Portugal), un bosque productor altamente organiza- do, localizado en la costa centro-occidental de Portugal (39° 50’ N, 8° 57’W, 30 - 50 m.s.n.m.) y que está compuesto esencialmente por el pino marítimo Pinus pinaster. La PV irrumpió en un área homogénea poblada por pinos juveniles. La abundancia y riqueza de aves fue estimada por medio de conteos por puntos en el área infestada y en dos áreas similares no infestadas. Los conteos fueron realizados en las cuatro estaciones, cubriendo todas las etapas del ciclo anual de la polilla y fueron repetidos durante dos años. La riqueza de recogedores del dosel fue mayor en el área de la PV que en un área adyacente no infestada. Sólo dos especies respondieron numéricamente al incremento de abundancia de insectos: el mirlo común Turdus merula y el carbonero común Parus major. Así, la comunidad de paseriformes res- pondió sólo en menor grado a la irrupción de la PV. Tres factores podrían explicar los resultados: (i) la comunidad de aves consiste, en su mayoría, en residentes territoriales o migratorios de corta distancia en las cuales su escaso rango de dispersión podría limitar la probabilidad de respuesta a una irrupción localiza- da. (ii) Las larvas de la procesionaria del pino tienen pelos urticantes que son considerados un mecanis- mo de defensa repelente contra depredadores vertebrados, reduciendo así el número de especies que po- drían reaccionar a altas densidades de orugas. (iii) La estructura simple de la vegetación del bosque, con parcelas homogéneas de pinos juveniles pequeños, excluye el establecimiento de las aves que anidan en cavidades que constituyen gran parte de los recogedores del dosel, además de la mayoría de las especies que han sido registradas como depredadores de T. pityocampa. Los resultados indican que este impor- tante defoliador mediterráneo podría tener efectos positivos en los recogedores del dosel y en algunas aves con capacidad de funcionar como depredadores de sus larvas. Palabras clave: comunidad de aves, insecto defoliador, irrupción de insectos, cambios en el ciclo de vida, bosque de pino mediterráneo, respuesta numérica, conteo por puntos.

INTRODUCTION having a major impact on the bird community structure (Holmes et al., 1986). This phe- Tree canopy insects are generally consid- nomenon was also observed in North Euro- ered as an important food item for most forest pean deciduous forests, although at a somewhat birds (e.g. Buckner and Turnock, 1965; Gui- smaller scale (Hogstad, 2005). However, in tián, 1985; Poulin and Lefebvre, 1996; Hogstad, forests from more southern latitudes, includ- 2005). In temperate forest ecosystems, some ing the Mediterranean area, there is limited in- of these folivorous species are able to cycli- formation on how a bird community responds cally reach outbreak numbers and cause ex- to irruptions of insect defoliators. tensive defoliation (Myers, 1998; Bjørnstad et The pine processionary moth (Thaume- al., 2002; Tenow et al., 2007), a phenomenon topoea pityocampa, Lepidoptera: Notodonti- which is also known in other forest ecosys- dae) is an important pine defoliator in the tems, although not so well studied (Van Bael Mediterranean region, and there is evidence of et al., 2004). In temperate deciduous forests cyclic outbreaks (Hódar and Zamora, 2004; in North America, the sudden impulse of food Robinet, 2006). This univoltine species spends caused by Lepidoptera outbreaks significant- the pupal stage in the ground during the spring. ly affects abundances of many bird species, Adults emerge in the summer and live for a few

Ardeola 56(2), 2009, 189-203 PASSERINE BIRDS AND THE PINE PROCESSIONARY MOTH 191 days, just enough for reproduction. Female liators through severe defoliation by late instar moths of this species lay a single batch of eggs, aposematic caterpillars (Pelech and Hannon, and larvae hatch about one month later, devel- 1995). However, in spite of the importance of oping throughout the winter (between Septem- T. pityocampa as a widespread forest defolia- ber and March) (OEPP/EPPO, 2004). Howev- tor, studies on the responses of the bird com- er, in 1997, a population of T. pityocampa with munity to high and low densities of this pest, a temporally shifted life cycle was recorded for are still scarce (but see Barbaro et al., 2008). the first time in a restricted area of the Nation- The irruption of the SP in a localized patch al Pine Forest of Leiria. Larval development of the forest, in an area where previous out- of this novel population occurs during the sum- breaks by defoliators are unknown (informa- mer instead of during the winter, and so this tion provided by the National Forest Services), population will be referred to as the Summer offered us an opportunity to assess how the bird Population (SP). Since its discovery, the SP has community of Mediterranean pine forests re- been observed every year in the same responds to outbreaks of a common insect defo- stricted area, causing visibly high levels of de- liator. Thus, in the present paper we character- foliation (own observations) and attaining high- ize the passerine community in the pine er densities than the Winter Population (WP) plantations where the SP established, and in- in the same area (Pimentel et al., 2006). vestigate if birds are able to respond to the ir- The pine processionary moth has aposemat- ruption of the shifted population of T. pityocam- ic gregarious caterpillars, with conspicuous pa. Accordingly, we compare bird richness and hairs and urticant setae in the last two instars abundance in the area of the irruption of the of development. These characteristics are con- SP, with similar uninfested forest areas. Pre- sidered as effective repellent defences dictably, the unexpected food source and de- against most bird predators (e.g. Bowers and foliation caused by a T. pityocampa outbreak Farley, 1990; Lindström et al., 2001; Exnerová should affect some, but not all, of the guilds et al., 2007). This way, it is expected that T. comprising the community, and therefore we pityocampa early instar larvae will constitute examine the effects of the SP outbreak sepa- a food source for avian predators, but preda- rately for each foraging guild. tion of later urticant instar larvae and pupae should be restricted to a few species that are able to overcome its defences. In fact, MATERIALS AND METHODS González-Cano (1981) found that T. pityocampa early larvae instars are commonly found The National Pine Forest of Leiria is locat- in the stomach contents and excrement of a ed 150 km north of Lisbon, covering 11,023 large number of bird species in an outbreak sit- ha in a coastal dune system (39º 50´ N, 8º 57 uation, especially in the family Paridae. ´W, 30 - 50 m a.s.l.). About 80 % of this area However, predation of later instar larvae was is managed to produce high quality timber. mostly restricted to cuckoos (Clamator glan- The pinewood is divided into 334 rectangular darius and Cuculus canorus), and great tits plots (management units) of 30 to 40 ha each (Parus major). The Eurasian hoopoe (Upupa covered mostly by even-aged monocultures of epops) is the only known predator of T. pity- maritime pine (Pinus pinaster) (for a more de- ocampa pupae (Battisti et al., 2000). This char- tailed description of the area see Pimentel et acteristic of T. pityocampa also leads to the hy- al., 2006). pothesis that an outbreak will have a negative Shortly after the first report of the occur- effect on the bird community due to the de- rence of the SP in September 1997 by the Na- crease in abundance of palatable insect defo- tional Forest Services, a survey was made cov-

Ardeola 56(2), 2009, 189-203 192 PIMENTEL, C. and NILSSON, J. Å.

ering all the area of the Leiria Forest to deter- mine the distribution of the SP outbreak, and select the areas for the bird surveys. During the winter 1997/98, the presence of SP larval nests was assessed by a group of three persons, each following separated transects of about 100 m in each one of the forest plots. The existence of plots with high levels of defoliation associated with the presence of the SP was also recorded. This preliminary survey showed that SP larvae were mostly restricted to plots aged between 5 and 20 years, located at the south end of the Leiria Forest, the area where the SP was initially detected, and were absent out- side this area. High levels of tree defoliation (plots with trees suffering from 100 % of defoliation) in the Leiria Forest were only observed in the SP distribution area associated with the presence of its larval nests. Thus, bird abundance and richness were compared between SP infested area (I) and two other similar, non-infested areas of young plots located in the north (NI1) and centre (NI2) of the forest (NI2 was located 7 km north and south, respectively, of the other two areas). The three forest areas were similar in relation to tree age (Kruskal-Wallis test: H2 = 1.08, P = 0.58; fig.1a), and tree density (Kruskal-Wal- lis test: H2 = 3.99, P = 0.14; fig. 1b). They were slightly different in relation to DBH Diameter at Breast Height (Kruskal-Wallis test: H2 = 7.90, P = 0.019), with slightly larger trees in NI1 (fig.1c). Management operations by the Forest services include periodical removal of the understory, making vegetation structure of FIG. 1.—Average (± SE) age (a), density (b), and the studied plots extremely simple. However, DBH (c) of pines in the three forest plots within the important differences were found in the tree National Pine Forest of Leiria where the bird sur- characteristics of the forest plots surrounding veys were made (- -), and in the forest plots imme- l the three studied areas (Kruskal-Wallis test: diately surrounding the studied plots (-n-). Data were supplied by the National Forest Services. age H2 = 20.3, P < 0.001; density H2 = 18.1, P [Media (± ES) de edad (a), densidad (b) y DAP (c) < 0.001; DBH H2 = 20.7, P < 0.001), with NI1 de pinos en las tres parcelas del Bosque Nacional and NI2 being surrounded by plots with older de Pinos de Leiria donde se efectuaron los recono- and larger trees in lower density (fig.1). This cimientos (-l-), y en las parcelas de bosque en la reflects the fact that the SP emerged in a ho- periferia inmediata a las áreas de estudio (-n-). Da- mogeneous area of young plantations within tos facilitados por el Servicio Nacional Forestal.] the forest (Pimentel et al., 2006).

Ardeola 56(2), 2009, 189-203 PASSERINE BIRDS AND THE PINE PROCESSIONARY MOTH 193

SP larvae hatch between mid July and begin- sessed, and so the defoliation with other ori- ning of August and larval development takes gin, including the WP and any other insect place during the summer. Larval processions species. These surveys were made in March of occur in October and early November (own ob- each year, just after the end of the WP larval pe- servations), when larvae leave the tree canopy riod, and about 5 months after the end of the SP to pupate into the ground. The pupal period be- larval period. Nests from the two populations comes longer in this population, lasting the are easily distinguishable since SP larvae weave whole winter and part of the spring, until the very loose nests that at the time of the year when appearance of imagoes in May to June. Bird the surveys were conducted looked older than abundances and richness were assessed through- the ones from the WP. In each one of the three out the year, covering all SP life stages. The areas of the bird counts, five spots were select- presence of passerine birds was assessed through ed randomly. In each one of those spots, an area 10 minute, 50 m radius point counts (Bibby et of about 0.07 ha was marked and all the trees al., 1992). In each of the areas, 12 point count inside this area were counted and observed with stations were located along a transect of about binoculars for checking for T. pityocampa nests 2,000 m, separated by a distance of 150 - 200 and any other defoliators. Defoliation was es- m. Each of these stations was located at least timated in the following categories: 1: 0 - 33 %, 100 m, inside the forest plot. Abundances were 2: 34 - 67 %, 3: 68 - 100 %. estimated in two time periods: between The statistical analyses were performed us- March 1998 – January 1999, and between Oc- ing SYSTAT 11. In order to test for spatial and tober 1999 – June 2000. In each of the time pe- temporal differences in bird richness and abun- riods, the visits to the point count stations were dance, a repeated measures ANOVA model was made in four distinct seasons: early March used with two grouping factors –area and sea- (Spring = Sp), during SP pupal period; late June son and with bird counts from the two years (Summer = Su), when SP imagos were avail- (i.e. the repeated measure) as the dependent able; late October to early November (Autumn variable. Abundance analyses only include bird = A), at the end of SP larval period when lar- species with more than 10 registrations. On ac- vae had reached their largest size; January (Win- count of the non-continuous integers and some ter = Wi), also during the SP pupal period. Vis- zero counts, the bird counts were trans- its to the stations of each transect were made in formed by (x+1)0.5 (Snedecor and Cochran, the same day at dawn. Days with strong winds 1980). Differences between mean values were and rain were avoided. As the three studied ar- compared using the Tukey test for unequal sam- eas were flat and vegetation structure very simple sizes. For controlling of Type I error, a se- ilar, the detectability of birds was assumed to quential Bonferroni-Holm procedure (Holm, be equal in all areas. 1979) was used for adjusting the significance Bird species were assigned to four different level (at 0.05) for each of the factors (area foraging groups according to literature, main- and season) and interaction, in multi-test ANO- ly Carrascal et al. (1997): bark foragers (BF), VA`s of bird abundances (different guilds ground feeders (GF), canopy gleaners (CG) and different bird species). and understory gleaners (UG). The residential status of each species was also assessed: residents (R) potentially occurring in the area all RESULTS year, migrants wintering in the area (W) and migrants breeding in the area (B). WP nests were observed all over the forest, In the spring of 2000 the distribution and lev- together with other tree defoliators, mainly the el of damage caused by the SP was again as- common pine sawfly Diprion pini (L.) and

Ardeola 56(2), 2009, 189-203 194 PIMENTEL, C. and NILSSON, J. Å. brown-tail moth Euproctis chrysorrhoea (L.) The UG was the second least important forag- (affecting Arbutus unedo). However, the latter ing group, in abundance (Tukey test: P < 0.001 two species caused lower levels of defoliation for all comparisons), and in number of species (less than 30 % in less than 1 % of trees attacked). (4). The GF had the highest abundances and The surveys made in 2000 confirmed that the the largest number of species (13), followed by SP was only present in area I (% attacked the CG (Tukey test: GF > CG P = 0.015) with trees: mean ± SD, 27.93 ± 21.79, n = 5; level 7 species (table 1; appendix A). of defoliation: 0.73 ± 0.71, n = 5). The only oth- In the two most abundant guilds, richness er significant defoliator was T. pityocampa WP varied according to the area, however in the on area NI1 and NI2 (% attacked trees: NI1 = case of GF, number of species was higher in 1.92 ± 2.56, n = 5, NI2 = 7.22 ± 5.01, n = 5; lev- NI2, while in the case of the CG it was higher el of defoliation: NI1 = 0.03±0.05, n = 5, NI2 in I. In the case of the GF richness also changes = 0.10 ± 0.08, n = 5). However, both the % of seasonally, being higher in the spring and sum- attacked trees and level of defoliation were sig- mer, a pattern also observed for the total rich- nificantly lower than the ones caused by the ness (table 2). SP in I (Kruskal-Wallis test: % attacked trees: There were no statistically significant dif- H2 = 6.552, df = 2, P = 0.038; level of defolia- ferences in the overall bird abundance be- tion H2 = 7.647, P = 0.022). tween areas (table 1). However, differences Twenty-six passerine bird species were were found among the seasons, with abun- recorded in the young maritime pine planta- dances being higher during spring and sum- tions studied. Of these, 84.6 % (22 species), mer than during autumn and with the lowest which accounted for 98.7 % of all registers, abundances in winter. This pattern of season- were permanent residents or short distance al variation in abundances was found both in migrants. Exceptions were three species of the GF and UG guilds. However, in the BF long range migratory wintering birds; chif- and CG guilds, abundances did not differ be- fchaff (Phylloscopus collybita), redwing (Tur- tween seasons (table 1). Few species with res- dus iliacus) and fieldfare (Turdus pilaris) ident status, opposed the general trend and all with low abundances and the common had higher abundances during the autumn. cuckoo (Cuculus canorus) being the only long Those were greenfinches (Carduelis chloris), range migratory breeding species recorded, robins (Erithacus rubecula), sardinian war- also in low abundance. Half of the species blers (Sylvia melanocephala) and spotless (14), accounting for 92.4 % of all registers, starlings (Sturnus unicolor), indicating some were recorded in the studied areas during all migratory influxes during the autumn (ap- the four seasons. The three most abundant pendix A). species; the wren (Troglodytes troglodytes), Regarding the spatial variation of individ- the chaffinch (Fringilla coelebs) and the coal ual species, the bark forager short-toed tit (Periparus ater), accounting for 50 % of treecreeper (Certhia brachydactyla) had a high- all registrations, were all permanent residents er abundance in NI1 than in the other two plots. (appendix A). The ground feeders wood lark (Lullula arborea) We found differences in the distribution of and serin (Serinus serinus), had highest bird abundance per feeding guild (repeated abundance in NI2. Furthermore, blackbirds measure ANOVA for differences in passerine (Turdus merula) and great tits (Parus major) guilds: F3,572 = 3.56, P = 0.014). The BF group increased in abundance more than two times included only two species and had lower abun- in I than in the NI1 and NI2 (appendix A). This dances than all the other three foraging groups difference was mostly due to higher abundances (Tukey test: P < 0.001 for all comparisons). in the summer in the infested area in the case

Ardeola 56(2), 2009, 189-203 PASSERINE BIRDS AND THE PINE PROCESSIONARY MOTH 195

TABLE 1

Occurrence of birds belonging to four different foraging groups in three different areas of young pines in the National Pine Forest of Leiria during the surveys in spring (Sp), summer (Su), autumn (A) and winter (Wi). Repeated measures analyses of variance tested the differences in bird abundances, between the three areas and the four seasons. Repeated measures were the two periods: March 1998 – January 1999 and Oc- tober – 1999 June 2000. * Denotes significant values after Bonferroni-Holm correction. Obs. denotes the total number of observations. For a species account of the different foraging groups see appendix A. [Ocurrencia de aves pertenecientes a cuatro diferentes grupos de forrajeo en tres áreas diferentes de pinos juveniles en el Bosque Nacional de Pinos de Leiria durante los reconocimientos de primavera (Sp), verano (Su), otoño (A) e invierno (Wi). Los análisis de la varianza con mediciones repetidas comparan las diferencias en abundancia de aves entre las tres áreas y las cuatro estaciones. Las mediciones repetidas fueron realizadas en dos periodos: marzo 1998 – enero 1999 y octubre 1999 – junio 2000. * Seña- la valores significativos después de la corrección de Bonferroni-Holm. Obs. indica el número total de observaciones. Para descripciones de las especies en diferentes grupos de forrajeo, véase el apéndice A.]

Guild Source Repeated measures ANOVA Tukey test, P Obs. d.f. F P Bark foragers Area 2,132 3.086 0.049 - 34 Season 3,132 0.013 0.998 - Area x Season 6,132 1.137 0.345

Ground feeders Area 2,132 4.478 0.013 - 834 Season 3,132 41.344 <0.001* Sp, Su > A> Wi, 0.03 Area x Season 6,132 1.275 0.273

Canopy gleaners Area 2,132 2.707 0.070 - 718 Season 3,132 0.876 0.455 - Area x Season 6,132 0.756 0.606

Understory gleaners Area 2,132 1.505 0.226 - 441 Season 3,132 30.943 <0.001* Sp, Su > A > Wi, < 0.02 Area x Season 6,132 3.129 0.007*

Total Area 2,132 0.011 0.989 - 2027 Season 3,132 32.796 >0.001* Sp, Su > A > Wi, 0.005 Area x Season 6,132 0.772 0.593 of the blackbird, and in summer and autumn in pa in a maritime pine forest, in spite of the over- the case of the great tit (fig.2). all richness and abundance of birds being similar in infested and in non-infested areas. Two bird species had a much higher abundance in DISCUSSION the infested than in the non-infested areas: the blackbird and the great tit. The significant in- In the present study we found some response teraction between area and season indicates of the passerine community to a localized ir- that the differences in abundance between the ruption of a novel population of T. pityocam- areas are largest in summer in the case of the

Ardeola 56(2), 2009, 189-203 196 PIMENTEL, C. and NILSSON, J. Å.

TABLE 2

Bird richness in the two most important foraging groups in three different areas of young pines in the National Pine Forest of Leiria during the surveys in spring (Sp), summer (Su), autumn (A) and winter (Wi). Repeated measures analyses of variance tested the differences in bird richness, between the three areas and the four seasons. Repeated measures were the two periods: March 1998 – January 1999 and Oc- tober 1999 – June 2000. * Denotes significant values after Bonferroni-Holm correction. [Riqueza de aves en los dos grupos más importantes de forrajeo, en tres áreas diferentes, con pinos juveniles en el Bosque Nacional de Pinos de Leiria durante los reconocimientos de primavera (Sp), verano (Su), otoño (A) e invierno (Wi). Los análisis de la varianza con mediciones repetidas comparan las diferencias en riqueza de especies entre las tres áreas y las cuatro estaciones. Las mediciones repetidas fueron realizadas en dos periodos: marzo 1998 – enero 1999 y octubre 1999 – junio 2000. * Señala valores significativos de la corrección de Bonferroni-Holm.]

Guild Source Repeated measures ANOVA Tukey test, P d.f. F P Ground feeders Area 2,132 7.531 0.001* NI2 > NI1, 0.003 Season 3,132 32.436 < 0.001* Sp, Su > A > Wi, 0.001 Area x Season 6,132 2.603 0.020* ≤

Canopy gleaners Area 2,132 4.248 0.016* I > NI2, 0.035 Season 3,132 1.933 0.127 - Area x Season 6,132 1.204 0.308

Total Area 2,132 2.879 0.060 - Season 3,132 29.704 < 0.001* Sp, Su > A> Wi, 0.001 Area x Season 6,132 2.121 0.055 ≤ blackbird. This was also observed in the sum- majority of bird species inhabiting these forests mer and autumn in the case of great tits, al- migrated annually and could detect outbreaks though not statistically significant after the during their northward movements to breeding Bonferroni-Holm correction (appendix A, fig. areas in the spring (Buckner and Turnock, 1965; 1). This is the time when imagoes and larvae Holmes et al., 1986; Crawford and Jennings, of the SP are available in the field. Further- 1989; Haney, 1999; Hogstad, 2005). The bird more, bird richness in the bird guild most like- communities of the Mediterranean forests con- ly to be affected by a defoliator –the canopy sidered in the present work are constituted most- gleaners– proved to be higher in the infested ly by territorial residents or short distance mi- area than in the nearby NI2. grants occurring in the area all year. More The bird community structure found on the restricted movements of this type of birds might present study is rather different to the ones from decrease their probability to find a localized in- North-American and Northern European sub- sect outbreak. Migratory wintering birds that boreal forests, where numerical responses of arrive at the end of the summer, could poten- bird communities to forest insect irruptions have tially take advantage of the abundance of SP been previously detected. In these cases, the caterpillars. However, only a few of these species outbreaking species were univoltine, with lar- were recorded and then in small numbers in the val development occurring during spring. The young plantations of the Leiria Forest.

Ardeola 56(2), 2009, 189-203 PASSERINE BIRDS AND THE PINE PROCESSIONARY MOTH 197

FIG. 2.—Average (± SE) number of blackbirds (a) and great tits (b) per count point in three different plots of the National Pine Forest of Leiria (NI1 -n-, NI2 -∂- and I -¡-) obtained during four different seasons in two years (between March 1998 – January 1999; and October 1999 – June 2000). [Media (± ES) del número de mirlos (a) y carboneros (b) por punto de conteo en tres parcelas diferentes del Bosque Nacional de Pinos de Leiria (NI1 -n-, NI2 -∂- and I -¡-) obtenidos durante cuatro estaciones diferentes en dos años (entre marzo 1998 – enero 1999 y octubre 1999 – junio 2000).]

Another factor that may possibly limit the These surroundings might have accounted for numerical response of birds to the SP irrup- the tendency for higher abundances of GF in tion is the vegetation structure of the forest. NI2 (table 1). Furthermore most of the canopy The existence of large (old) trees, a high num- gleaners guild is constituted by cavity nesters ber of dead trees, high tree species richness who need large trees and snags to breed. This and understory vegetation generally positive- guild is the most likely to respond to an out- ly influence total bird richness and abundance break of a forest defoliator, and has most of in maritime pine forests (Moreira et al., 2003; the species registered as predators of T. pity- Barbaro et al., 2005). In the Leiria Forest, con- ocampa (González-Cano, 1981). sisting of pure stands of maritime pine, Forest areas of more diverse age structure plantations are regenerated after clear-cuts had no or low SP levels (Pimentel et al., 2006). and no snags or residual trees are left. Under- The extreme simplicity of the SP establishment story vegetation is periodically removed in area may have decreased the diversity and abun- plots with young trees to avoid competition. dance of the bird fauna, leading to a compar- Trees with a small DBH and the lack of un- atively low predation pressure on moths and derstory probably account for the low num- caterpillars of this novel Lepidoptera popula- ber of species and low abundance of the BF tion, thereby allowing it to become established. and UG found in the present work. In fact, The aposematism and urticant defences of high numbers of the short-toed treecreepers T. pityocampa also makes this species distinct and wood larks were recorded in NI1 and NI2, from other outbreaking species in which nu- respectively. NI1 was surrounded by forest merical responses of birds have been observed plots of older and larger trees than the in- so far, which are geometrid or tortricid species fested area, and NI2 had several neighbor for- with naked and palatable caterpillars such as est plots which had recently been clear cut. the spruce budworm (Choristoneura fumifera-

Ardeola 56(2), 2009, 189-203 198 PIMENTEL, C. and NILSSON, J. Å. na) (Crawford and Jennings, 1989), the elm earthworms, it can incorporate large quantities spanworm (Ennomos subsignarius) (Haney, of all life stages of Lepidoptera in its diet (Igle- 1999), the winter moth (Operophtera bruma- sias et al., 1993). High abundances of black- ta) and the autumnal moth (Epirrita autumna- birds coincided with the time when imagos of ta) (Hogstad, 2005). However, a tendency for the SP emerge from the ground. Adult moths higher richness in the canopy gleaners Paridae emerge before dusk, they crawl to the nearest in the SP infested area indicate an increase in branch to stretch their wings and wait until night resources for this family, since the increase in to start dispersion and sexual activity (own ob- energy for a bird community can lead to a servations). Thus, during this period they are greater number of species independent of the probably vulnerable to predation by the ground number of individuals (Hurlbert, 2004). feeding blackbird. The numerical response of great tits to the SP was somewhat expected, since it is one of the passerines that are able to prey on hairy ACKNOWLEDGEMENTS.—The authors would like and urticating caterpillars (Royama, 1970) to thank the National Forest Services for allowing and use all instars of T. pityocampa caterpil- the work to be conducted in the Leiria Forest, and J. lars as food sources during the winter, mak- P. Pina, R. Rufino and R. Neves from “Mãe d`Agua” ing them the main avian predator of such cater- for conducting the bird counts. E. Ruelas translated pillars (González-Cano, 1981). This bird is the parts in Spanish, and suggestions by two anony- able to open holes in the nests of late instar mous referees greatly improved an earlier version of caterpillars, extracting its larvae and consum- the manuscript. This work was supported by the Por- ing the soft tissues while avoiding ingesting tuguese Foundation for Science and Technology through funding from the PRAXXIS XXI pro- the hairs (González-Cano, 1981). The ob- gramme, and with a PhD grant refª PRAXXIS XXI served increase in abundance in the SP infest- /BD/18119/98 conceded to C. Pimentel. ed area may be due to higher reproductive rates of local breeding couples (Pimentel and Nilsson, 2007). At the time of breeding sea- BIBLIOGRAPHY son SP imagos were available, and adult moths can constitute an important food source in BARBA, E. and GIL-DELGADO, J. A. 1990. Seasonal Mediterranean ecosystems for provisioning variation in nestling diet of the great tit Parus ma- great tit nestlings (Barba and Gil-Delgado, jor in orange groves in eastern Spain. Ornis Scan- 1990). It may also be due to young birds be- dinavica, 21: 296-298. ing attracted from nearby areas by the local- BARBARO, L., PONTCHARRAUD, L., VETILLARD, F., ized abundance of caterpillars during the sum- GUYON, D. and JACTEL, H. 2005. Comparative re- mer, since this highly territorial passerine sponses of bird, carabid, and spider assemblages disperses primarily during its first year of life to stand and landscape diversity in maritime pine plantations forests. Ecoscience, 12: 110-121. (Greenwood et al., 1979). BARBARO, L., COUZI, L., BRETAGNOLLE, V., NEZAN, The high abundance of blackbirds in the in- J. and VETILLARD, F. 2008. Multi-scale habitat se- fested area during the summer is interesting lection and foraging ecology of the Eurasian since, to our knowledge, blackbirds have not hoope (Upupa epops) in pine plantations. Bio- been recorded as predators of T. pityocampa. diversity and Conservation, 17: 1073-1087. However, a massive influx of blackbirds has BATTISTI, A., BERNARDI, M. and GHIRALDO, C. 2000. been registered in a localised outbreak of the Predation by the hoopoe (Upupa epops) on pu- jack pine budworm (Choristoneura pinus) pae of Thaumetopoea pityocampa and the likely (Mattson et al., 1968; cited in Otvos, 1979). In influence on other natural enemies. BioControl, fact, although this species feeds mostly on 45: 311-323.

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BIBBY, C. J., BURGUESS, N. D. and HILL, D. A. 1992. HOGSTAD, O. 2005. Numerical and functional re- Bird census techniques.Academic Press. London. sponses of breeding passerine species to mass BJØRNSTAD, O. N., PELTONEN, M., LIEBHOLD, A. occurrence of geometrid caterpillars in a sub- M. and BALTENSWEILER, W.2002. Waves of larch alpine birch forest: a 30-year study. Ibis, 147: budmoth outbreaks in the European Alps. Sci- 77-91. ence, 298: 1020-1023. HOLM, S. 1979. A simple sequentially rejective mul- BOWERS, M. D. and FARLEY, S. 1990. The behavior tiple test procedure. Scandinavian Journal of Sta- of gray jays, Perisoreus canadensis, towards palat- tistics, 6: 65-70. able and unpalatable Lepidoptera. Animal Behav- HOLMES, R. T., SHERRY, T. W. and STURGES,F. W. iour, 39: 699-705. 1986. Bird community dynamics in a temperate BUCKNER, C. H. and TURNOCK, W. J. 1965. Avian deciduous forest: long-term trends at Hubbard predation on the larch sawfly, Pristiphora Brook. Ecological Monographs, 13: 299-320. erichsonii (HTG.), (Hymenoptera: HURLBERT, A. H. 2004. Species-energy relationships Tenthredinidae.). Ecology, 46: 223-236. and habitat complexity in bird communities. Ecol- CARRASCAL, L. M., POTTI, J. and SÁNCHEZ-AGUA- ogy Letters, 7: 714-720. DO, F. J. 1987. Spatio-temporal organization of IGLESIAS, D. J., GIL-DELGADO, J. A. and BARBA, E. the bird communities in two Mediterranean mon- 1993. Diet of Blackbird nestlings in orange groves: tane forests. Holarctic Ecology, 10: 185-192. seasonal and age-related variation. Ardeola, 42: CRAWFORD, H. S. and JENNINGS, D. T. 1989. Preda- 113-119. tion by birds on the spruce budworm Choristoneu- LINDSTRÖM, L., ALATALO, R .V., LYYTINEN, A. and ra fumiferana: functional, numerical and total re- MAPPES, J. 2001. Predator experience on cryptic sponses. Ecology, 70: 152-163. prey affects the survival of conspicuous EXNEROVÁ, A., Sˇ TYS, P., FUCˇIKOVÁ, E., VESELÁ, S., aposematic prey. Proceedings of the Royal Society SVÁDOVÁ, K., PROKOVÁ, M., JAROSˇIK, V., FUSCH, of London, Series B, 268: 357-361. R. and LANDOVÁ, E. 2007. Avoidance of MOREIRA, F., DELGADO, A., FERREIRA, S., BOR- aposematic prey in European tits (Paridae): RALHO, R., OLIVEIRA, N., INÁCIO, M., SILVA, J. S. learned or innate? Behavioral Ecology, 18: 148- and REGO, F. 2003. Effects of prescribed fire on 156. vegetation structure and breeding birds in young GONZÁLEZ-CANO, J. M. 1981. Predación de Pinus pinaster stands of northern Portugal. For- processionaria del pino por vertebrados en la zona est Ecology and Management, 184: 225-237. de Mora de Rubielos (Teruel). Boletin de la MYERS, J.H. 1998. Synchrony in outbreaks of for- Estacion Central de Ecología, 10: 53-77. est Lepidoptera: a possible example of the Moran GREENWOOD, P. J., HARVEY, P. H. and PERRINS, C. effect. Ecology, 79: 1111-1117. M. 1979. The role of dispersal in the great tit OEPP/EPPO 2004. Diagnostic protocols for regu- (Parus major): the causes, consequences and her- lated pests Thaumetopoea pityocampa. Bulletin itability of natal dispersal. Journal of Animal Ecol- OEPP/EPPO, 34: 155-157. ogy, 48: 123-142. OTVOS, L. S. 1979. The effects of insectivorous bird GUITIÁN, J. 1985. Feeding regime of the passerine activities in forest ecosystems: an evaluation. In, community in a montane forest of the Western J. G. Dickson, R. N. Conner, R. R. Fleet, J. C. Cantabrian Mountains. Ardeola, 32: 155-172. Kroll, and J. A. Jackson, (Eds.): The role of in- HANEY, J. C. 1999. Numerical responses of birds to sectivorous birds in forest ecosystems, pp. 341- an irruption of elm spanworm (Ennomos subsig- 374. Academic Press. New York. narius [Hbn.]; Geometridae: Lepidoptera) in old- PELECH, S. and HANNON, S. J. 1995. Impact of tent growth forest of Appalachian Plateau, USA. For- caterpillar defoliation on the reproductive suc- est Ecology and Management, 120: 203-217. cess of black-capped chickadees. Condor, 97: HÓDAR, J. A. and ZAMORA, R. 2004. Herbivory and 1071-1074. climatic warming: a Mediterranean outbreaking PIMENTEL, C. and NILSSON, J. -Å. 2007. Response caterpillar attacks a relict, boreal pine species. of Great Tits Parus major to an irruption of a Pine Biodiversity and Conservation, 13: 493-500. Processionary Moth Thaumetopoea pityocampa

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population with a shifted phenology. Ardea, 95: SNEDECOR, G. W. and COCHRAN, W. G. 1980. Sta- 191-199. tistical methods, Seventh Edition. Iwoa State Uni- PIMENTEL, C., CALVÃO, T., SANTOS, M., FERREIRA, versity Press. Ames. C., NEVES, M. and NILSSON, J. -Å. 2006. Estab- TENOW, O., NILSSEN, A. C., BYLUND, H. and lishment and expansion of a Thaumetopoea pity- HOGSTAD, O. 2007. Waves and synchrony in Epir- ocampa (Den. & Schiff.) (Lep. Notodontidae) rita autumnata/Operophtera brumata outbreaks. population with a shifted life cycle in a produc- I. Lagged synchrony: regionally, locally and tion pine forest, Central-Coastal Portugal. Forest among species. Journal of Animal Ecology, 76: Ecology and Management, 233: 108-115. 258-268. POULIN, B. and LEFEVRE, G. 1996. Dietary relation- VAN BAEL, S. A., AIELLO, A., VALDERRAMA, A., ME- ships of migrant and resident birds from a humid DIANERO, E., SAMANIEGO, M. and WRIGHT, S. J. forest in central Panama. Auk, 113: 277-287. 2004. General herbivore outbreak following an El ROBINET, C. 2006. Mathematical modelling of in- Niño-related drought in a lowland Panamanian for- vasion processes in ecology: the pine procession- est. Journal of Tropical Ecology, 20: 625-633. ary moth as a case study. PhD dissertation. École des Hautes Études en Sciences Sociale. Paris. [Recibido: 17-07-2008] ROYAMA, T. 1970. Factors governing the hunting be- [Aceptado: 16-06-2009] havior and selection of food by the great tit (Parus major L.). Journal of Animal Ecology, 39: 619-668.

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APPENDIX A

Occurrence of bird species belonging to four different foraging groups in three different areas of young pines in the National Pine Forest of Leiria during the surveys in spring (Sp), summer (Su), autumn (A) and winter (Wi). The residential status of each species is denoted by R = resident; W = wintering and B = breeding. Repeated measures analyses of variance tested the differences in bird abundances, obtained by the point count method, between the three areas, the four seasons. Repeated measures were the two periods: March 1998 – January 1999 and October 1999 – June 2000. * Denotes significant values after Bon- ferroni-Holm correction. Obs. denotes the total number of observations. [Ocurrencia de especies de aves que pertenecen a cuatro diferentes grupos de forrajeo en tres áreas diferentes de pinos juveniles en el Bosque Nacional de Pinos de Leiria durante los reconocimientos de primavera (Sp), verano (Su), otoño (A) e invierno (Wi). El estatus de cada especie es señalado con R = residente, W = invernante y B = reproductor. Los análisis de la varianza de mediciones repetidas exami- naron las diferencias en abundancia de aves obtenidas mediante el método de conteo por puntos entre las tres áreas y las cuatro estaciones. Las mediciones repetidas se hicieron en dos periodos: marzo 1998 – enero 1999 y octubre 1999 – junio 2000. * Señala valores significativos después de la corrección de Bon- ferroni-Holm. Obs. indica el número total de observaciones.]

Species, res. Source Repeated measures ANOVA Tukey test, P Obs. status: season d.f. F P Bark foragers Certhia brachydactyla Area 2,132 7.532 0.001 * NI 1 > NI2, I, 0.003 21 R: Sp Su A Wi Season 3,132 1.002 0.394 - Area x Season 6,132 0.308 0.932

Dendrocopus major Area 2,132 1.144 0.322 - 13 R: Sp Su A Wi Season 3,132 1.731 0.164 - Area x Season 6,132 1.731 0.119

Ground feeders Carduelis chloris Area 2,132 2.520 0.084 - 29 R: Su A Wi Season 3,132 7.743 < 0.001 * A > Su, 0.004 Area x Season 6,132 0.827 0.551

Corvus corone Area 2,132 1.562 0.214 - 76 R: Sp Su A Wi Season 3,132 1.091 0.355 - Area x Season 6,132 2.671 0.018

Erithacus rubecula Area 2,132 0.987 0.375 - 185 R: Sp Su A Wi Season 3,132 24.652 < 0.001 * A > Sp, Su > Wi, 0.03 Area x Season 6,132 2.254 0.042

Fringilla coelebs Area 2,132 5.783 0.004 * NI1 > I, 0.045 355 R: Sp Su A Wi Season 3,132 73.531 < 0.001 * Sp, Su > A, Wi, < 0.001 Area x Season 6,132 4.480 < 0.001 *

Garrulus glandarius R: Sp; Su; A - - - - 5

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APPENDIX A CONT.

Species, res. Source Repeated measures ANOVA Tukey test, P Obs. status: season d.f. FP Lulula arborea Area 2,132 17.179 < 0.001 * NI2 > NI1, I, 0.001 29 R: Sp Su Wi Season 3,132 17.719 < 0.001 * Sp > Su, Wi, < 0.02 Area x Season 6,132 4.924 < 0.001 *

Picus viridis Area 2,132 15.242 < 0.001 * NI1, NI2 > I, 0.02 38 R: Sp Su A Wi Season 3,132 0.571 0.635 - Area x Season 6,132 3.267 0.005

Serinus serinus Area 2,99 8.478 < 0.001 * NI2 > NI1, I, 0.002 12 R: Sp Su Wi Season 2,99 1.985 0.119 - Area x Season 4,99 1.322 0.252

Sturnus unicolor R: A - - - - 4

Turdus iliacus W: A - - - - 9

Turdus merula Area 2,132 10.986 < 0.001 * I > NI1, NI2, 0.03 61 R: Sp Su A Wi Season 3,132 11.060 < 0.001 * Sp, Su > A, Wi, < 0.03 Area x Season 6,132 4.312 0.001*

Turdus pilaris W: A - - - - 3

Turdus viscivorus Area 2,66 8.708 < 0.001 * NI2,I > NI1, 0.05 28 R: Sp Su Season 1,66 28.286 < 0.001 * Su > Sp, < 0.001 Area x Season 2,66 8.970 < 0.001 *

Canopy gleaners Aegithalus caudatus Area 2,132 1.768 0.175 - 13 R: Sp Su A Wi Season 3,132 0.426 0.735 - Area x Season 6,132 0.380 0.891

Cuculus canorus B: Sp Su - - - 9

Parus ater Area 2,132 0.533 0.588 - 332 R: Sp Su A Wi Season 3,132 7.372 < 0.001 * Su > A, Wi, 0.03 Area x Season 6,132 1.970 0.074 Sp > A, 0.017≤

Parus cristatus Area 2,132 1.619 0.202 - 157 R: Sp Su A Wi Season 3,132 0.752 0.523 - Area x Season 6,132 0.267 0.952

Parus major Area 2,132 9.714 < 0.001* I > NI1, NI2; 0.001 126 R: Sp Su A Wi Season 3,132 2.585 0.056 - ≤ Area x Season 6,132 2.221 0.045

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APPENDIX A CONT.

Species, res. Source Repeated measures ANOVA Tukey test, P Obs. status: season d.f. FP Phyloscocus collybita W: A - - - - 5

Regulus ignicapillus Area 2,132 1.234 0.295 - 76 R: Sp Su A Wi Season 3,132 5.941 0.001 * Sp, Su > Wi, 0.003 Area x Season 6,132 0.886 0.507 ≤

Understory gleaners Silvia atricapilla R: Sp Su A - - - - 8

Sylvia melanocephala Area 2,132 0.642 0.528 - 14 R: Sp Su A Season 3,132 7.456 < 0.001* A > Sp, Su, 0.05 Area x Season 6,132 1.864 0.092

Sylvia undata Area 2,132 2.683 0.072 - 51 R: Sp Su A Wi Season 3,132 3.278 0.023 - Area x Season 6,132 3.191 0.006 -

Troglodytes troglodytes Area 2,132 3.573 0.031 - 368 R: Sp Su A Wi Season 3,132 30.148 < 0.001* Sp ,Su > A> Wi, < 0.001 Area x Season 6,132 1.742 0.116

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