population decline of the capercaillie tetrao urogallus … · 2020. 10. 6. · analizamos la...

POPUlATION DEClINE OF ThE CAPErCAIllIETETRAO UROGALLUS AQUITANICUS

IN ThE CENTrAl PyrENEES

DEClIVE POBlACIONAl DEl UrOGAllOTETRAO UROGALLUS AQUITANICUS EN lOS PIrINEOS CENTrAlES

Juan Antonio GIl1, Miguel Ángel GóMEZ-SErrANO2 *and Pascual lópez-lópez3

SUMMAry.—long-term monitoring of endangered birds is essential to estimate population trendsand to identify potential causes of population decline. This is particularly important for alpine birdsinhabiting mountain areas at the boundaries of their range. here we analyse the population trend ofCapercaillie in the Spanish Central Pyrenees based on annual surveys carried out between 2000 and2017. We found a significant population decline (around 58%) in the number of birds counted in leks.Most capercaillies inhabit coniferous forests of Black Pine with abundant Bilberry and rhododendronunderstorey. The number of males declined at lower altitudes and in more exposed orientations, in ascenario consistent with the differential rate of loss of habitat quality due to climate change. Wehypothesised that one of the main causes of the Capercaillie decline could be low breeding success(average annual productivity 0.67 chicks per female). In light of the decline rates observed, the Pyreneanpopulation should be relisted as endangered in the Spanish National Catalogue of Endangered Species.Affording a higher degree of protection should guarantee the adoption of management measures toreverse or slow down the general trend of decline of the species in the south of its range.—Gil, J.A.,Gómez-Serrano, M.Á. & lópez-lópez, P. (2020). Population decline of the Capercaillie Tetraourogallus aquitanicus in the Central Pyrenees. Ardeola, 67: 285-306.

Key words: alpine birds, breeding success, conservation, grouse, habitat preference, monitoring data,population trend, TrIM.

rESUMEN.—El seguimiento a largo plazo de las aves amenazadas es esencial para estimar las ten-dencias poblacionales e identificar las posibles causas de declive, siendo particularmente importante enel caso de las aves alpinas que habitan en áreas montañosas en los límites de su área de distribución.

Ardeola 67(2), 2020, 285-306 DOI: 10.13157/arla.67.2.2020.ra4

1 Fundación para la Conservación del Quebrantahuesos (FCQ), Plaza San Pedro Nolasco 1, 4-F,50001 Zaragoza, Spain.

2 Departament of Microbiology and Ecology, Faculty of Biological Sciences,University of Valencia, E-46100 Burjassot, Valencia, Spain.

3 Cavanilles Institute of Biodiversity and Evolutionary Biology, Terrestrial Vertebrates Group,University of Valencia, C/ Catedrático José Beltrán 2, E-46980 Paterna, Valencia, Spain.

* Corresponding author: [email protected]

Twitter: @FCQorg / @GomezSerrano_MA / @lopez_pascual

INTrODUCTION

European mountain birds are declining,mainly due to the high vulnerability of alpinehabitats to climate change and local land usepractices (Flousek et al., 2015; lehikoinen etal., 2019). The Western Capercaillie Tetraourogallus is a bird of conservation concern(Storch, 2007a) that is experiencing a severedecline in many regions of Europe (Moss etal., 2000; Storch, 2007a; Sirkiä et al., 2010;Ewing et al., 2012; Zawadzki & Zawadzka,2012; Eaton et al., 2015). The decline ofEuropean Capercaillie populations started inthe 20th century, beginning earlier in southernareas (Storch, 2007a), due to poor breedingsuccess and low recruitment rate (Obeso &Bañuelos, 2003; Jahren et al., 2016). Thelatter has been related to factors such ashabitat loss, habitat fragmentation, illegalhunting, climate change or increase of out-door recreation (Moss et al., 2001; Obeso& Bañuelos, 2003; Quevedo et al., 2006a;Thiel et al., 2008; Morán-luis et al., 2014).

The Capercaillie is a polygamous grousewith an ‘exploded’ lek breeding system i.e.males use communal display areas in thebreeding season (Wegge et al., 2013). leksoccur in forest habitats (Summers et al.,

2004a). The distribution of the Capercaillieis fundamentally linked to the taiga forests ofthe Eurasian area, although it also appears insome mountainous areas of the centre (Alps,Vosges and Jura), South (Cantabrian andPyrenean) and East (Balkans) of Europe(Storch, 2007a). The Spanish population ofCapercaillie is distributed across two mainareas: the Cantabrian range and the Pyrenees.Both areas represent the southwestern limitof the species’ global range, where it wasisolated after the last quaternary glaciationthat triggered their speciation (Canut et al.,2011). The Cantabrian population is repre-sented by the subspecies T. u. cantabricus(Storch et al., 2006), while that of the Pyre-nees is represented by the T. u. aquitanicus,a western lineage shared with the Balkans(Duriez et al., 2007; Bajc et al., 2011). Thedistribution of the Pyrenean Capercailliepopulation is approximately continuous inFrance, while in Spain it is fragmented intotwo areas: a small western core betweenNavarra and western huesca provinces anda much larger one from the “Cinca valley”in huesca to the “Alto Ter” in Catalonia(Andorra included, Ménoni et al., 2004).

In the Pyrenees, most studies of the popu-lation trend of the Capercaillie have been

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GIl, J.A., GóMEZ-SErrANO, M.Á. and lóPEZ-lóPEZ, P.286

Analizamos la tendencia poblacional del urogallo en los Pirineos centrales españoles a partir de investi-gaciones realizadas entre 2000 y 2017. Encontramos un declive significativo de la población (alrededordel 58%) en el número de aves contadas en las áreas de exhibición (lek). la mayoría de los urogalloshabitan bosques de coníferas de pino negro con una cobertura elevada de arándano y rododendro en elsotobosque. El número de machos disminuyó más rápidamente a altitudes más bajas y en orientacionesmás expuestas, en un escenario consistente con la tasa diferencial de pérdida de calidad del hábitatdebido al cambio climático. Nuestra hipótesis es que una de las principales causas del declive delurogallo podría ser un bajo éxito reproductivo (productividad media anual de 0,67 pollos por hembra).A la luz de las tasas de disminución observadas, debería cambiarse la categoría del Catálogo Españolde Especies Amenazadas de Vulnerable a En Peligro de Extinción. Esta consideración de un mayorgrado de protección legal debería garantizar la adopción de medidas de gestión para revertir o desace-lerar la tendencia general de declive de la especie en el sur de su área de distribución.—Gil, J.A.,Gómez-Serrano, M.Á. y lópez-lópez, P. (2020). Declive poblacional del urogallo Tetrao urogallusaquitanicus en los Pirineos centrales. Ardeola, 67: 285-306.

Palabras clave: aves alpinas, conservación, éxito reproductor, preferencias del hábitat, tetraónidas,tendencia poblacional, TrIM.

based on the comparison of the magnitudeof change between surveys every 5-10 years(Ménoni et al., 2004; Ballesteros et al., 2006).The first surveys of the Capercaillie popula-tion of the Spanish Pyrenees were conductedin the early 1980s. Subsequently, in 2005, anew estimate of the number of active lekswas made, including a count of the numberof males (Ballesteros et al., 2006). Althougha decline close to 40% in the number of malesbetween both surveys was observed, mostleks remained active. Nevertheless, both thedifferences in the area surveyed betweenthe two censuses (i.e., the number of knownand visited leks) and the absence of an inter-annual monitoring protocol, make it difficultto assess the degree of decline of the popu-lation in the Spanish Pyrenees.

The subspecies aquitanicus is cataloguedas “Vulnerable” in Spain in the National Cata-logue of Endangered Species. Since 2005,the Aragón region must implement a “Pyre-nean Capercaillie habitat Conservation Plan”which establishes measures to guarantee the

long-term viability of its populations. Thedevelopment of this plan requires studies ofthe population trend and reproductive successin this region of the Pyrenees (lorente et al.,2004; Gil & Alcántara, 2011). In this study,we analyse the population trend of the speciesin the Spanish Central Pyrenees (Aragón)based on interannual monitoring carried outover 18 years. We aimed to (1) estimate thepopulation trend of males and females in leks;(2) characterise breeding habitats; (3) assesshow different habitat types can affect declinerates; and (4) identify the relationship be-tween productivity and population decline.

METhODS

Study area

Our study was carried out in the CentralSpanish Pyrenees (huesca province, Ara-gón), specifically in the regions of Jacetania(Veral, Aragón Subordán and Aragón valleys),

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POPUlATION DEClINE OF CAPErCAIllIE IN PyrENEES 287

FIG. 1.—The study area in the Spanish Central Pyrenees.[Área de estudio en los Pirineos centrales españoles.]

Sobrarbe (Cinca and Cinqueta valleys) andribagorza (Esera and Noguera-ribagorzanavalleys). These areas are identified in thePyrenean Capercaillie habitat ConservationPlan in Aragón (Decree 300/2015). The planidentifies 25 Critical Areas (total = 24,476ha)that are defined as vital for the survival andconservation of the species (Figure 1).

In the Central Pyrenees, Capercaillies in-habit mature coniferous forests of montaneand subalpine areas, with preference for BlackPine Pinus uncinata, although they are alsopresent in other forests such as Scots PinePinus sylvestris or Silver Fir Abies alba, andoccasionally in reforestations of Europeanlarch Larix europaea and Spruce Picea abies(lorente et al., 2004; Guzman & Navascues,2006). From 2000 to 2017 we surveyedCapercaillie habitats during the courtshipperiod (late April – early June). Our surveysincluded direct and indirect bird observa-tions, including lekking sites and indirectevidence of bird presence (e.g. scat). Froman initial list of places with presence of thespecies, these surveys allowed us to increaseconsiderably the number of known leks.

Habitat characterisation and areaof occupation

To characterise habitat around leks, wecategorically classified forests according tothe dominant tree and understorey shrub spe-cies. For each lek site, the contiguous area ofsuitable forest with presence of Capercaillieswas mapped to obtain the extent of occur-rence. We also documented indirect evidenceof the species, such as tracks, feathers, orfaecal droppings (Moss et al., 2014).

Lek counts

Males and females were counted annually(2000-2017) at all leks on single visits from

late April to early June (Catusse & Novoa,1983). The lek location was based on his-torical information and surveys conducted inprevious years. We counted the number ofmales singing at each lek at sunrise (Catusse& Novoa, 1983). To determine the exact lo-cation of every lek, each season we visitedthe sites the afternoon before the count and,following male vocalisations, we locatedthe roosting tree that birds use during thenight close to the display territory (Wegge etal., 2013).

During visits, we also counted the numberof females that attended the lek. The num-ber of females counted in the leks may notreflect their actual abundance because theymay visit more than one lek during the lekkingseason and they only attend for short periods(Storch, 1997). Nevertheless, long-term seriesof female counts might provide valuable in-formation to estimate population trends.

Breeding success

Transects (rajala, 1974; leclercq, 1987;Canut et al., 1996) and dogs trained to flushfemales and any associated chicks were usedto estimate breeding success (Ellison, 1979;Ménoni, 1987; Wegge & Kastdalen, 2008).Breeding surveys were carried out from 2002to 2007 during late July and early August,coinciding with the chick-rearing period (Gil& Alcántara, 2011). We only surveyed areasof suitable habitat where the presence ofCapercaillie in the spring or in previous sum-mers was confirmed. In order to avoid dou-ble counts, transects were started at loweraltitudes than the sites used by capercaillies.Transects were carried out by a team of be-tween five and eight people that walked lineabreast separated from each other by 15-20metres. Transects with trained dogs werecarried out by two people. Surveys coveredthe entire forest area with suitable habitatfor Capercaillie at a slow speed, maintaining

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the altitudinal elevation and visual contactbetween the observers. Each plot was sur-veyed for three to four hours early in themorning.

Productivity was measured as the meannumber of chicks per female (including thosewith no chicks). We analysed the relation-ship between productivity and Capercaillieabundance measured as the number of full-grown birds. Following Summers et al.(2010), changes in density (i.e. the numberof full-grown males and females per 100ha)along transects were expressed as a per-centage change from one summer (year t) tothe next (year t + 1), and compared withproductivity in the previous summer (year t)in a linear regression analysis. Even thoughmale Capercaillies do not breed until theage of three or more (Wegge & larsen,1987; Storch, 1997, 2001), we assumed thatone– and two-year-old males could also bepart of the count at leks and summer counts(Wegge & larsen, 1987).

Trend analysis

We evaluated the Capercaillie populationtrend using TrIM software (Trend & Indicesfor Monitoring data, TrIM 3.54). TrIM is astatistical software developed for the analy-sis of long-term time series data from animalmonitoring programmes (Pannekoek & VanStrien, 2005). In recent years, TrIM has be-come one of the most used softwares for birdpopulation trend assessment (Gregory et al.,2009; Gregory & Van Strien, 2010; Flouseket al., 2015; lehikoinen et al., 2019). TrIMestimates annual population change indicesimplementing log-linear regression modelswith Poisson error terms that represent theeffect of change between years. The TrIMindex value at the first time point (or anotherpoint considered as the baseline year) is 1.0and it is taken as a reference for trends insubsequent years. The main advantages of

TrIM are: (1) correction for both overdis-persion and serial correlation; (2) incorpo-ration of significant change points in trends;and (3) analyses of time series counts withmissing observations (Pannekoek & VanStrien, 2005; Gregory & Van Strien, 2010).The latter is particularly advantageous whentime series are incomplete due to lack ofsampling, as occurred in some of our studyareas. To overcome this limitation, missingcounts for specific sites and years were esti-mated by TrIM from changes in all othersites (Gregory et al., 2005). We calculatedthe population trend from 2000 to 2017 usinga TrIM linear trend model with 2000 as thebase year. The goodness-of-fit of models wastested by Pearson’s Chi-squared statistic andby the likelihood ratio test. We started theanalysis with a model with change points ateach year, and used the stepwise selectionprocedure to identify change points withsignificant changes in slope (based on Waldtests and a significance-level threshold valueof 0.05; Pannekoek & van Strien, 2005). Inorder to avoid underestimation of standarderrors, we took into account overdispersionand serial correlation in TrIM options for allmodels. We used three categorical variables:(1) habitat type (i.e., Scots Pine or BlackPine forests); (2) Orientation (Northern vs.other orientations), and (3) Elevation (aboveor below the median altitude of leks; 1,900m).Wald tests (provided by TrIM) were usedto assess the significance of change pointsand to test for differences in trends betweencovariate categories. A set of 16 modelswas generated: eight for each sex group,including the combination of categoricalvariables (i.e., habitat, altitude, orientation)and a model without covariates. We selectedthe most parsimonious model using theAkaike information criterion correctedfor small samples (AICc), and we rescaledmodel values using the minimum AICc toprovide evidence of the relative support foreach model: ΔAICc = AICc – AICc min. We

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consider that models with a ΔAICc < 2 havestrong support, and those with ΔAICc > 10have less support (Burnham and Anderson,1998). According to Pannekoek & van Strien(2005), trends were classified taking intoaccount the slope imputed (i.e., multiplica-tive value) and the standard error providedby TrIM in the following six categories:Steep decline, Moderate decline, Stable,Moderate increase, Strong increase, andUncertain.

rESUlTS

We monitored 39 different leks attendedby at least one male during the breeding sea-son. These leks were visited during at leastfour years between 2000 and 2017 (mean8.92 ± 3.88 visits/lek over the 18 years of thestudy period). Overall, the sampling effortwas of 348 count stations, with an averageof 19.33 ± 7.63 leks visited per year. A totalof 34 transects were carried out in 11 dif-ferent localities during 2002-2007. The totalarea surveyed annually ranged between 349and 501ha.

Habitat characterisation

leks were mainly located in continuousBlack Pine forests (79.5%). We located someleks in mixed Black Pine and Silver Firforest (5.1%). The remaining leks were inScots Pine forests, often mixed with BlackPine, Silver Fir or Common Beech Fagussylvatica. Five shrub species were identifiedas the main structural species of the under-storey (Supplementary Material, Appendix1, Figure A1). At 84.6% of the leks, the un-derstorey was characterised by a mixture ofBilberry Vaccinium myrtillus and rhododen-dron Rhododendron ferrugineum (Supple-mentary Material, Appendix 1, Figure A2).leks were located at altitudes between 1,550and 2,180m a.s.l. (median = 1,900m) (Sup-

plementary Material, Appendix 1, FigureA3). Northern orientations (N, NW, NE)were more frequent (71.8% of leks) thansouthern, eastern or western orientations.

The extent of occurrence of the Caper-caillie in huesca was 2,621ha (Figure 1).This area is divided into 37 fragments, nearlyall of them (94.9%) including only one lekand two (5.1%) including two leks. The meanarea of these fragments was 70.8 ± 37.2ha(N = 37). There was no relationship betweenthe size of these fragments and the meannumber of displaying males (Spearmancorrelation, r = 0.2370, N = 37, P = 0.158).Nevertheless, the maximum number of dis-playing males recorded in the study correlatedwith fragment size (Spearman correlation,r = 0. 3879, N = 37, P = 0. 018; Figure 2).

Lek trend and summer counts

leks were attended by an average of1.71 ± 0.91 males and 1.37 ± 0.40 females(only leks with a positive count for each sexwere considered), with a maximum of sevenmales and six females per lek. The annualpercentage of visited leks with bird presenceshowed a significant negative trend duringthe study period for both males (r2 = 0.9105,N = 18, P < 0.0001) and females (r2 = 0.3432,N = 18, P = 0.006). At the end of the studyperiod (2017) more than half of the leks(54.1%) had been deserted by males (r2 =0.9121, N = 18, P < 0.0001) (Figure 3). A to-tal of 17 males and 37 females were countedin the summer transects. The average densityof capercaillies was 2.89 ± 3.10 adults/100ha(males: 0.68 ± 1.13, females: 2.21 ± 2.57,N = 34).

The number of capercaillies in leks andthe density of birds estimated in summertransects around these leks in the same yeardid not show a significant relationship(Spearman correlations, males, r = 0.3441,N = 21, P = 0.127; females, r = 0. 2910, N =18, P = 0.241).

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FIG. 2.—Correlation between the maximum number of displaying Capercaillie males in leks and thearea of habitat patches with presence of the species around each lek (period 2000-2017, Aragón, CentralSpanish Pyrenees).[Correlación entre el número máximo de machos de urogallo censados en los lek y el área de fragmentoscon presencia de la especie alrededor de cada lek (período 2000-2017, Pirineos centrales, Aragón, Es-paña).]

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FIG. 3.—Percentage of active leks for males (black line), females (grey line) and accumulated percentageof deserted leks (dotted line) over time in Aragón (Central Spanish Pyrenees).[Evolución temporal del porcentaje de leks activos para los machos (línea negra), hembras (línea gris) yel porcentaje acumulado de leks desertados (línea de puntos) en los Pirineos centrales (Aragón, España).]

Productivity

Of the females we counted in summertransects, 45.95% (N = 37) were accompa-nied by chicks (mean = 2.05 chicks/female).Considering the total number of femalescounted in transects, the average productivitywas 0.95 ± 1.31 chicks per female (N = 37).Mean annual productivity from 2002 to 2007was 0.67 ± 0.79 chicks per female (range =0–2.13; N = 6).

There was a positive but non-significantcorrelation between the percentage change inthe number of males at leks and the produc-

tivity in the previous summer (t = 0.8366,N = 10, P = 0.427; Supplementary Material,Appendix 1, Figure A4). This relationshipwas negative but non-significant for the in-dices of abundance for Capercaillie betweensummer counts (t = –0.6765, N = 19, P =0.508; Supplementary Material, Appendix 1,Figure A4).

Population trend

For both sexes, the top-ranked modelsclassified the trend as a moderate decline

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TABlE 1

Summary of TrIM model results for the period 2000-2017. The results of all models are shown foreach sex group. Abbreviations: OD, overdispersion. SC, serial correlation. lr, likelihood ratio.AICc, Akaike information criterion corrected for small samples. AICw, Akaike weight. OMS, OverallMultiplicative Slope imputed. SE, Standard error. *P < 0.05; **P < 0.01.

Model OD SC LR AICc ΔAICc AICw OMS ± SE Trend class Males Altitude 0.59 0.283 203.33 –400.56 0.00 0.47 0.9382 ± 0.0082 Moderate decline**

Orientation 0.59 0.258 205.09 –398.80 1.76 0.19 0.9385 ± 0.0081 Moderate decline**

Orientation + 0.597 0.286 203.79 –397.88 2.69 0.14 0.9382 ± 0.0083 Moderate Altitude decline**

No covariates 0.583 0.273 211.82 –398.18 2.38 0.13 0.9312 ± 0.0088 Steep decline*

habitat 0.597 0.281 208.47 –395.42 5.14 0.04 0.9362 ± 0.0083 Moderate decline**

habitat + 0.586 0.269 201.18 –394.49 6.08 0.03 0.9362 ± 0.0082 Moderate Altitude decline**

habitat + 0.589 0.268 203.38 –392.29 8.28 0.01 0.9365 ± 0.0083 Moderate Orientation decline**

habitat + Moderate Orientation + 0.588 0.268 199.7 –387.61 12.95 0.00 0.9360 ± 0.0082 decline** Altitude

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TABlE 1 (cont.)

[Resumen de los resultados de los modelos calculados en TRIM para el período 2000-2017. Se muestranlos resultados de todos los modelos para ambos sexos. Abreviaturas: OD, sobredispersión. SC, corre-lación serial. LR, Razón de máxima verosimilitud. AICc, criterio de información de Akaike corregidopara muestras pequeñas. AICw, peso de Akaike. OMS, pendiente general multiplicativa imputada porTRIM. SE, error estándar. *P < 0,05; **P < 0,01.]

Model OD SC LR AICc ΔAICc AICw OMS ± SE Trend class Females No covariates 0.930 0.021 277.86 –274.14 0.00 0.42 0.9724 ± 0.0134 Moderate decline*

Altitude 0.933 0.016 274.86 –273.03 1.11 0.26 0.9646 ± 0.0118 Moderate decline**

habitat 0.897 –0.036 267.17 –272.72 1.42 0.22 0.9673 ± 0.0125 Moderate decline**

habitat + 0.907 –0.006 267.42 –270.25 3.89 0.07 0.9650 ± 0.0116 Moderate Altitude decline**

Orientation 0.939 0.010 279.78 –268.11 6.03 0.02 0.9679 ± 0.0130 Moderate decline*

habitat + 0.909 –0.020 260.86 –264.81 9.33 0.00 0.9651 ± 0.0133 Moderate Orientation decline**

Orientation + 0.948 0.006 274.77 –262.90 11.24 0.00 0.9692 ± 0.0138 Moderate Altitude decline**

habitat + Moderate Orientation + 0.925 –0.035 255.16 –256.15 17.99 0.00 0.9647 ± 0.0136 decline** Altitude

(Table 1). The top-ranked model for malesshowed greater decline (annual change =–6.18%) than females (annual change =–2.76%). Despite these differences in declinerates, both sexes showed a similar percentageof population decline in 2017 compared tothe beginning of the study period (2000-2017), with a population reduction greaterthan 57% in both cases (males, 57.84%; fe-males, 57.61%) (Figure 4).

The best model for males included theeffect of altitude (Wald = 11.70, df = 4, P =0.020). A second model with similar ex-planatory value (ΔAICc < 2) included site

orientation instead, although this variable hada non-significant effect. Our modelling re-sults for females produced three best modelswith similar support: the model without co-variates and two models with altitude andhabitat, respectively. In the latter two models,although covariates were included, their effectwas not significant (altitude, Wald = 8.92,df = 5, P = 0.112; habitat, Wald = 12.58,df = 7, P = 0.083). There were three yearswith significant points of change for males(2007, Wald = 21.33, df = 2, P < 0.0001;2009, Wald = 7.57, df = 2, P = 0.028; 2016,Wald = 10.45, df = 2, P = 0.005) and two for

females (2000, Wald = 3.86, df = 1, P =0.0495; 2010, Wald = 4.83, df = 1, P = 0.028;2011, Wald = 4.31, df = 1, P = 0.038). Forthe most parsimonious models for males theestimated decline was greater for popula-tions located below 1,900m, especially during2010-2016 and for more exposed orienta-tions (Figure 5).

DISCUSSION

long-term monitoring of endangered birdsis essential to estimate population trends andto identify potential causes of population de-

cline. This is particularly important for alpinebirds inhabiting mountainous areas at theedge of their range (lehikoinen et al., 2019).here we provide updated information on thedistribution of the endangered Capercailliein the Pyrenees, where only 28 leks had pre-viously been surveyed in the Central Pyrenees(Aragón region) (Ballesteros et al., 2006).

We found that the mean number of bothmales and females attending leks was low,compared with other sectors of the Pyrenees(Ménoni, 1994; Canut et al., 2006) as wellas with Northern European populations(Angelstam, 2004; Zawadzki & Zawadzka,2012). Similarly, the density of birds in the

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FIG. 4.—TrIM imputed index of the Capercaillie breeding population in Central Spanish Pyreneesfrom 2000 to 2017. Trends of males and females are shown separately based on a linear model withoutcovariates. Errors bars indicate standard errors.[Tendencia de la población reproductora de urogallo en los Pirineos centrales españoles entre 2000y 2017 según el índice imputado por el programa TRIM. Se muestra la tendencia de machos y hembraspor separado con base en un modelo lineal sin covariables. Las barras verticales muestran el errorestándar.]

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FIG. 5.—TrIM imputed index according to the two top-ranked models for males over time. The top-ranked model included altitude (upper figure) and the second one included orientation (lower figure).[Tendencia poblacional de los machos de urogallo según el índice imputado por el programa TRIMpara los dos modelos mejor clasificados. El modelo mejor clasificado incluía la covariable altitud(figura superior) y el segundo modelo la covariable orientación (figura inferior).]

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summer counts was lower than elsewhere intheir ranges (Moss & Oswald, 1985; Mietti-nen et al., 2008) and even within the Pyre-nees (Fernández-Olalla et al., 2012).

Studies in Northern and Central Europehave shown that male Capercaillies establishtheir home ranges around leks in spring(Wegge & larsen, 1987; rolstad et al., 1988;Storch, 1997; Eliassen & Wegge, 2007), andthat territory size is inversely related to theproportion of optimum habitat within them(Wegge & rolstad, 1986). likewise, the num-ber of male birds that attend leks dependson the quality and quantity of the surroundingforest habitats (Picozzi et al., 1992; Storch,1995a; Angelstam, 2004; Summers et al.,2004a). Indeed, we found that the maximumnumber of males recorded in leks increasedwith the area of favourable habitat aroundthem. Based on such evidence, it has beensuggested that territorial spacing behaviourmight limit the number of males at leks(Wegge & rolstad, 1986). Nevertheless, thislimitation in the number of males as a resultof the spacing pattern could result fromhabitat fragmentation or habitat alterationby human activities, since leks in pristineforests can be attended by a greater numberof males coming from more distant territo-ries (rolstad & Wegge, 1987; Wegge et al.,2003; rolstad et al., 2009). In the case ofCentral Pyrenees, habitat fragmentation ismainly due to human activities (Canut etal., 2011), so that the number of males thatcan attend leks is generally limited by theavailability of suitable habitat, which is, inturn, constrained by climatic limitations.

Trend

Since 2000, the number of lekking Caper-caillie has been monitored annually at 39sites. Our estimate of the male populationwas 89 ± 9 birds in Aragón in 2000 (Supple-mentary Material, Appendix 1, Figure A5).

This Central Spanish Pyrenean populationdecreased to only 37 ± 6 males at the end ofthe study period (2017). Although the numberof females counted in the leks may not reflecttheir actual abundance (Storch, 1997), ourmodels estimate that the initial population(2000) of females that visited leks was 45 ± 9individuals and only 19 ± 4 at the end of thestudy period.

Our results show a significant populationdecline of Capercaillie in the Central Pyre-nees during 2000-2017, with a decline ofmore than 57% on the number of birdscounted in leks. This negative trend recordedin the central Pyrenees is consistent with thegeneral decline of Capercaillie populationsall over Europe (Moss et al., 2000; Storch,2007b; Sirkiä et al., 2010; Zawadzki & Za-wadzka, 2012; Morán-luis et al., 2014; Eatonet al., 2015).

We observed that females declined morequickly than males in the first years of study,although the overall percentage of changewas similar by the end of the period (Figure4). Nevertheless, the annual decline rate washigher in males (–6.18% per year) than fe-males (–2.76%). Moss et al. (2000) observeda different pattern in Scotland, with fasterdecline observed in females. Even thoughthe sex ratio in chicks is higher for females(Wegge, 1980; Moss & Oswald, 1985;hornfeldt et al., 2001), they suggest that thegreater longevity of cocks is the probableexplanation.

The Cantabrian Capercaillie populationhas declined by 70% in the number of malesat leks between 1981 and 2003 (Pollo et al.,2005; Storch et al., 2006). This steep declinecaused its recent relisting (2018) as “criti-cally endangered” in Spain in the NationalCatalogue of Endangered Species. To date,the population of the Pyrenean subspecieshas been regarded as declining more slowly.For instance, Ménoni et al. (2004) estimatedonly a 5.5% decline in range in the Pyre-nees between 1975 and 2000. Similarly,

Ballesteros et al. (2006) estimated that91.7% of historical leks were still occupiedin 2005. Nonetheless, the rate of decline isdifferent when considering the number ofbirds attending leks. 44% of the leks of thePyrenean mountain range showed a declinein the number of males between 1990 and2002, with a maximum reduction in theFrench Central Pyrenees (62% of leks de-clining; Ménoni et al., 2004). This declinewas estimated as close to 40% in the case ofthe Spanish Pyrenees, a rate obtained fromthe comparison of 1983 and 2005 surveys(Ballesteros et al., 2006). A more accurateestimate of the population trend, based onthe interannual monitoring of adult Caper-caillie density for the period 1988-2010,found a 4% annual decrease of adult birds inthe Catalonian Pyrenees (Fernández-Olallaet al., 2012).

It is notable that most decline rates for thePyrenees refer to periods up to the beginningof the 2000s. Therefore, the decline reportedin the Central Pyrenees should be signifi-cantly higher than that observed in this study,since the reduction of 57% between 2000and 2017 must be added to the 40% regis-tered between 1983 and early 2000s. The sub-species aquitanicus is listed as “Vulnerable”in Spain under the National Catalogue ofEndangered Species. In light of the declinerates observed since the 1980s, which seemto have accelerated in recent years, the na-tional threat category of the species shouldbe reviewed, since the criteria for a higherlevel of protection are likely to be met.

Breeding success

One of the factors that have been most fre-quently invoked as a cause of the decline ofCapercaillie is low breeding success (Moss etal., 2000; Obeso & Bañuelos, 2003; Baineset al., 2004; Summers et al., 2004b; Jahrenet al., 2016). Our results show low produc-

tivity during the study period (0.95 ± 1.31chicks per female). Although only a shorttime series is available, it is noteworthy thatin two of the five years of monitoring theproductivity was zero chicks per female(mean annual productivity = 0.67 chicks perfemale). Despite limited sample size, thislow productivity is similar to that of otherdeclining populations, such as in Scotland(Summers et al., 2004b), and is within thegeneral context of declining productivity ofthe species in European populations (re-viewed by Jahren et al., 2016). Focusing onthe Spanish Pyrenees, the low success hasbeen documented since the late 1980s andproductivity has fallen from 1.3 to fewer than0.5 chicks per female between 1988 and 2001(Ménoni et al., 2004). Moreover, breedingsuccess is slightly higher than that docu-mented in the Catalan Pyrenees, where pro-ductivity was 0.82 chicks per female during1993-2013 (Pimenta et al., 2014).

As reported by Moss & Oswald (1985) fora Scottish Capercaillie population, neitherthe summer counts nor the number of malesat leks were related to productivity in theprevious year. Nonetheless, this relationshipcould be subject to high interpopulation vari-ability, since these variables were correlatedat a nearby Scottish location (Summers etal., 2010).

Some authors have suggested that globalwarming could reduce Capercaillie breedingsuccess (Moss et al., 2001; Selås et al., 2011;Jahren et al., 2016), and this seems to havebeen a major cause of decline of regionalCapercaillie populations (Moss et al., 2001).Nevertheless, the mechanisms of this rela-tionship are not yet understood (Jahren etal., 2016). Contrary to this prediction, inless temperate regions the effect may be theopposite. For instance, Wegge & rolstad(2017) claim that in Finland breeding successin the boreal forest was enhanced in warmersprings. Nevertheless, it has been suggestedthat the most southern populations and those

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of Atlantic climates are the most vulnerableto climate change (Storch, 2007). Indeed,models based on climate scenarios for the21st century forecast a reduction rangingbetween 99% and 100% in the potential dis-tribution of the species in Spain for the pe-riod 2041-2070 (Araújo et al., 2011).

In addition, predation is the most im-portant cause of natural mortality in theCapercaillie, especially in pre-adult stages(Tornberg, 2001; reif et al., 2004; Wegge &Kastdalen, 2007), and so is one of the mainfactors that reduce productivity (Marcströmet al., 1988).

Habitat

In the Spanish Central Pyrenees, we foundthat the most Capercaillies inhabit coniferousforests of Black Pine with abundant Bilberryand rhododendron understorey. This pref-erence for boreal and montane coniferousforests with abundant Bilberry is consistentwith Capercaillie habitat selection in mostEuropean populations (Storch, 1993, 2001;Wegge & Kastdalen, 2008). For the Pyreneanmountain range, it indicates that the speciesuses a considerable variety of forest habitats(Monzón, 1981; Ballesteros et al., 2006;Ménoni, 2011), although in the southernmountains it is usually associated with BlackPine forests (Ménoni, 1994; Ménoni et al.,2004; Pascual-horta & Saura, 2008). Theresults of our models indicate that the num-ber of males declined faster at lower alti-tudes and in more exposed orientations (i.e.,south, east and west). This asymmetricalpopulation decline is of conservation con-cern under the expected scenario of climatechange, as marginal habitats are desertedfirst following the loss of their quality asbreeding areas. In addition, this decline in-creased towards the end of the study period,which might be interpreted as an accelera-tion of the consequences of climate change.

Bilberry is a key component of the Caper-caillie diet in the Eurosiberian region (Mosset al., 1979; Storch, 1995b; Quevedo et al.,2006b; Blanco-Fontao et al., 2010), so Bil-berry management is the cornerstone ofCapercaillie conservation. The Capercaillieis strongly linked with Bilberry distributionin the Pyrenees (Ménoni, 2011; Montané etal., 2016). Campión et al. (2011) claim thatin some areas in the southern Pyrenees, Bil-berry can be replaced in the diet by BearberryArctostaphylos uva-ursi. We found that theBearberry was present in 23.1% of the placeswith presence of Capercaillie, but only inthree such places (7.7%) was the Bilberryabsent. Bearing in mind that two of theselatter sites have recently lost their lek, it isclear that such habitat is used marginally bythe Capercaillie in the Central Pyrenees.

Habitat management

habitat management is essential for theconservation of the European Capercailliepopulations (Suchant & Braunisch, 2004;hancock et al., 2011; Broome et al., 2014).Baines et al. (2004) suggest suitable habitatrequires a minimum of 15-20% Bilberryground cover. In the Pyrenees, it has beenestimated that the optimal coverage of Bil-berry for Capercaillie should be 50-80%(Campión et al., 2011). Based on Pyreneanstudies, Montané et al. (2016) stated thatcanopy cover and understorey composition(particularly rhododendron cover) determinethe cover and fruit production of Bilberry.They concluded that reducing rhododendroncover has a strong positive effect on Bilberrycover and fruit production. Nevertheless,rhododendron clear-cutting experimentsconducted in the region have not apparentlyinfluenced Capercaillie density and clear-cutshave been more beneficial for wild ungu-lates and livestock (Camprodon et al., 2016).Other authors suggest that the elimination ofundergrowth could have negative conse-

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quences, such as an increase in predationrates, mainly of chicks (Wegge et al., 2005;Kvasnes & Storaas, 2007). Despite thesecontroversial results, it has been suggestedthat the species needs a certain level of spa-tial heterogeneity (Canut et al., 2011). Forinstance, Mikoláš et al. (2017) showed that,in primary forests of the Carpathian Moun-tains, a disturbance regime of variable inten-sity is required to generate diverse habitatssuitable for Capercaillie, and they concludethat natural disturbance should be mimickedas a conservation tool in protected areas.

Previous studies have shown that predatorcontrol may increase Capercaillie produc-tivity (Marcström et al., 1988; Kauhala et al.,2000; Baines et al., 2004; Summers et al.,2004b). For instance, Moreno-Opo et al.(2015) showed that the breeding success ofa Pyrenean population of Capercaillie wasenhanced in areas where carnivores wereremoved. Nevertheless, some authors havequestioned the effectiveness of predator con-trol and have highlighted the occurrence ofundesired side-effects (rushton et al., 2006;Woodroffe & redpat, 2005). These limi-tations are added to the negative view thatsociety has of predator control, so that alter-native management strategies must be pro-moted (Moreno-Opo et al., 2015). Generalistmesopredators can reach high densities in theabsence of top-down control (Kämmerle etal., 2017), so one of the proposed alterna-tives to predator control is the recovery ofapex predators (ripple et al., 2014; Moreno-Opo et al., 2015). The Eurasian lynx waspresent in the Pyrenees until the early-nine-teenth century (Clavero & Delibes, 2013) and,according to some sources, until the earlytwentieth century (Jiménez et al., 2018).Therefore, its reintroduction in the Pyreneesmight have a positive effect on Capercailliebreeding success through a reduction in po-tential predators, even considering that lynxcan also prey on capercaillies (Andrén &liberg, 2015).

Predators may contribute to the local ex-tinction of Capercaillie populations whenthey act on populations affected by lack ofboth suitable habitat and connectivity (Weggeet al., 1992; Kämmerle et al., 2017). Further-more, this negative effect of predation couldbe compensated under optimal habitat con-ditions, so conservation actions should beaimed at improving both habitat connectivityand quality (Sirkiä et al., 2012). It has beensuggested that increased woodland size andreduction of fragmentation might decreasethe presence of some predators associatedwith the interface between open habitats andwoodland (Wegge et al., 1992; Summers etal., 2004b). These measures could be effec-tive against corvids, which have been docu-mented as predators of Capercaillie nests(Storch, 2001; Baines et al., 2004; Summerset al., 2004b).

Finally, in addition to the above-men-tioned factors (i.e., habitat loss, predation,climate change), human disturbance could becontributing to Capercaillie decline (Storch,2013). human presence alters Capercailliebehaviour by increasing stress levels (Sum-mers et al., 2007; Thiel et al., 2007; Jenni-Eiermann & Arlettaz, 2008; Thiel et al.,2008). Outdoor recreation has a negativeimpact on Capercaillie habitat selection(Suárez-Seoane & García-rovés, 2004; Mosset al., 2014). It has been shown that somerecreational infrastructures (e.g. cross-coun-try trails and ski trails) reduce habitat occu-pancy in winter (Canut et al., 2004; Jenni-Eiermann & Arlettaz, 2008; Canut et al.,2011; Coppes et al., 2017). In the same way,birds avoid infrastructures such as mountainbike trails in summer (Coppes et al., 2017).We have documented the decline in thenumber of birds in some leks where humandisturbance has increased in recent years,especially in the form of winter activitiessuch as cross-country skiing and snow-shoeing. The control of outdoor recreationin Capercaillie habitats is probably one of

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the main challenges that managers shouldaddress to improve the conservation status ofthe species.

In summary, considering the high rates ofdecline observed in the Central Pyrenees, andthose documented in other sectors of themountain range, we suggest reconsidering theprotection status of the subspecies in regionaland national legislation. Pyrenean popula-tions of Capercaillie should be relisted as‘endangered’ in the Spanish National Cata-logue of Endangered Species. Such con-ferring of a higher degree of protection shouldguarantee the adoption of management mea-sures to reverse or slow down the generaltrend of decline of the Capercaillie in thesouth of its range.

ACKNOWlEDGEMENTS.—We would like to thankall the staff of the Foundation for the Conserva-tion of Bearded Vulture and particularly GonzaloChéliz, óscar Díez, Gerardo Báguena, Juan CarlosAscaso and Carlos Pérez. Surveys were partiallyfunded by the Aragón regional Government andFundación Biodiversidad. This paper complieswith current laws in Spain. Two anonymous re-viewers made valuable comments that improvedan earlier version of the manuscript.

AUThOr CONTrIBUTIONS.—M.A.G.-S. andJ.A.G. formulated the questions; J.A.G. collecteddata; J.A.G. and M.A.G.-S. designed methods;M.A.G.-S. analysed the data; all authors con-tributed to the visualization and data presenta-tion; M.A.G.-S. led the writing of the article;M.A.G.-S. and J.A.G. write the initial draft; P.l.-l.performed the critical review of the manuscriptand contributed to the drafting of the final versionof the manuscript. All authors gave final approvalfor publication.

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SUPPlEMENTAry ElECTrONIC MATErIAl

Additional supporting information may befound in the on-line version of this paper. Seethe volume 67(2) on www.ardeola.org

Submitted: June 26, 2019Major revisión: October 21, 2019

Second version arrived: December 17, 2020Accepted: February 26, 2020

Editor: Cristián Estades

Ardeola 67(2), 2020, 285-306


SUPPLEMENTARY ELECTRONIC MATERIAL ARDEOLA 67(2)

POPULATION DECLINE OF THE CAPERCAILLIE TETRAO

UROGALLUS AQUITANICUS IN THE CENTRAL PYRENEES

DECLIVE POBLACIONAL DEL UROGALLO TETRAO UROGALLUS AQUITANICUS

EN LOS PIRINEOS CENTRALES

Juan Antonio GIL1, Miguel Ángel GÓMEZ-SERRANO2,*and Pascual LÓPEZ-LÓPEZ3

1 Fundación para la Conservación del Quebrantahuesos (FCQ), Plaza San Pedro Nolasco 1, 4-F, 50001 Zaragoza, Spain. 2 Departament of Microbiology and Ecology, Faculty of Biological Sciences, University of Valencia, E-46100 Burjassot, Valencia, Spain. 3 Cavanilles Institute of Biodiversity and Evolutionary Biology, Terrestrial Vertebrates Group, University of Valencia, C/ Catedrático José Beltrán 2, E-46980 Paterna, Valencia, Spain.

* Corresponding author. [email protected]

Twitter: @FCQorg @GomezSerrano_MA @lopez_pascual

APPENDIX 1

Figure A1. Main structural plant species of the understorey at Capercaillie leks in Central Pyrenees (Aragón, Spain).

Figura A1. Principales especies de plantas estructurales del sotobosque en los ‘leks’ de los Pirineos centrales (Aragón, España).

0%

10%

20%

30%

40%

50%

60%

70%

80%

90%

Vacciniummyr6llus

Rhododendronferrugineum

Arctostaphylosuva-ursi

Juniperuscommunis

Buxussempervirens

percen

tageofleks

frequencyofoccurrenceofunderstoreyshrubspeciesinleks

Figure A2. Combinations of understorey plant species present at Capercaillie leks in Central Pyrenees (Aragón, Spain). Abbreviations: Vm, Vaccinium myrtillus; Rf, Rhododendron ferrugineum; Jc, Juniperus communis; Au, Arctostaphylos uva-ursi; Bs, Buxus sempervirens.

Figura A2. Combinaciones de especies de plantas del sotobosque presentes en los ‘leks’ del urogallo en los Pirineos centrales (Aragón, España). Abreviaturas: Vm, Vaccinium myrtillus; Rf, Rhododendron ferrugineum; Jc, Juniperus communis; Au, Arctostaphylos uva-usi; Bs, Buxus sempervirens.

0%

10%

20%

30%

40%

50%

60%

70%

Rf,Vm Rf,Vm,Jc,Au

Jc,Bs Jc,Au Jc,Bs,Au Rf,Vm,Jc,Bs,Au

percen

tageofleks

understoryshrubspeciesinleks

Figure A3. Altitudinal distribution of Capercaillie leks in Aragón (Central Pyrenees, Spain) during 2000-2017.

Figura A3. Distribución altitudinal de los ‘leks’ de Urogallo en los Pirineos centrales (Aragón, España) entre 2000 y 2017.

0

2

4

6

8

10

12

1500 1600 1700 1800 1900 2000 >2100

numbe

rofleks

Al8tudem

Figure A4. Percentage change in the Capercaillie abundance index on transects (upper figure) and at leks (lower figure) in relation to productivity (i.e., chicks per female) in Central Pyrenees (Aragón, Spain).

Figura A4. Porcentaje de cambio en el índice de abundancia de urogallo en los transectos (figura superior) y ‘leks’ (figura inferior) en relación con la productividad (número de pollos por hembra) en los Pirineos centrales (Aragón, España).

y=-9.9232x+3.4978

-150

-100

-50

0

50

100

150

200

0 1 2 3 4percen

tcha

nge

produc8vity

y=8.7562x-32.666

-120

-100

-80

-60

-40

-20

0

20

40

0 1 2 3 4

percen

tcha

nge

produc8vity

Figure A5. Total numbers of birds imputed by TRIM in the Capercaillie breeding population in Central Pyrenees (Aragón, Spain) during 2000-2017. Trends are shown by sex based on a linear model without covariates. The Total line refers to the sum of the females and males imputed by the models. Error bars indicate standard errors.

Figura A5. Tendencia del número de aves reproductoras de urogallo en los Pirineos centrales (Aragón, España) en el periodo 2000-2017 a partir del número de aves totales imputadas por el programa TRIM. Se muestra por separado la tendencia del total de aves para cada sexo según un modelo lineal sin covariables. La línea de individuos totales se refiere a la suma de los valores de las hembras y machos imputados por los modelos. Las barras verticales indican el error estándar.

0

20

40

60

80

100

120

140

160

2000 2002 2004 2006 2008 2010 2012 2014 2016

es8m

ated

num

bero

fbird

sFemalesMalesTotal

population decline of the capercaillie tetrao urogallus … · 2020. 10. 6. · analizamos la...

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