ippi2011.pdf

Geographical variation in the vocalizations of thesuboscine Thorn-tailed Rayadito Aphrastura

spinicaudaSILVINA IPPI,1* RODRIGO A. VASQUEZ,1 WOUTER F. D. VAN DONGEN1,2 & ILENIA LAZZONI1

1Departamento de Ciencias Ecologicas, Instituto de Ecologıa y Biodiversidad, Facultad de Ciencias,

Universidad de Chile, Las Palmeras 3425, Nunoa, Santiago, Chile2Konrad Lorenz Institute of Ethology, Department of Integrative Biology and Evolution, University of Veterinary

Medicine, Savoyenstrasse 1a, 1160 Vienna, Austria

Structural variation in acoustic signals may be related either to the factors affectingsound production such as bird morphology, or to vocal adaptations to improve soundtransmission in different environments. Thus, variation in acoustic signals can influenceintraspecific communication processes. This will ultimately influence divergence in allo-patric populations. The study of geographical variation in vocalizations of suboscinesprovides an opportunity to compare acoustic signals from different populations, withoutadditional biases caused by song learning and cultural evolution typical of oscines. Theaim of this study was to compare vocalizations of distinct populations of a suboscine spe-cies, the Thorn-tailed Rayadito. Four types of vocalizations were recorded in five popula-tions, including all three currently accepted subspecies. Comparisons of each type ofvocalization among the five populations showed that some variation existed in the repeti-tive trill, whereas no differences were found among alarm calls and loud trills. Variationin repetitive trills among populations and forest types suggests that sound transmission isinvolved in vocal differences in suboscines. Acoustic differences are also consistent withdistinguishing subspecies bullocki from spinicauda and fulva, but not the two latter sub-species from each other. Our results suggest that the geographical differentiation invocalizations observed among Thorn-tailed Rayadito populations is likely to be a conse-quence of different ecological pressures. Therefore, incipient genetic isolation of thesepopulations is suggested, based on the innate origin of suboscine vocalizations.

Keywords: acoustic adaptation hypothesis, bird morphology, Chile, Passeriformes.

Bird acoustic signals are essential in reproductiveevents (e.g. mating and territorial defence; Searcy &Andersson 1986, Catchpole 1987, Collins 2004), aswell as in anti-predator and social communicationsuch as alarm calls and contact calls (Marler 1955,2004, Magrath et al. 2007), and their diversificationcan be an important factor in the radiation of spe-cies, particularly in passerines (Nottebohm 1972,Endler 1992, Podos et al. 2004a). Song diversifica-tion can be linked to a number of different factors,

such as morphological adaptation, acoustic adapta-tion and species recognition (Ryan & Brenowitz1985, Seddon 2005) as well as stochastic processes(Irwin et al. 2008). This is particularly important inisolated populations, in which studies have reportedthe loss of functionality of territorial songs (Baker1994) and the simplification of songs (Hamao &Ueda 2000). Animals in isolated populations canalso lose the ability to recognize predators if theyare historically absent (Maloney & McLean 1995,Griffin et al. 2000, Beauchamp 2004) and as aconsequence modify or lose their alarm calls (Gill &Sealy 2004).

Bird vocalizations can be divided into two cate-gories, songs and calls. Songs are signals that tend

*Corresponding author.Email: [email protected]

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Ibis ª 2011 British Ornithologists’ Union

Ibis (2011), 153, 789–805

to be long and complex and are generally producedby males during the breeding season. In contrast,calls are shorter, simpler and are produced by bothsexes throughout the year (Catchpole & Slater2008). Bird vocalizations can be adjusted to theacoustics of the natural environments to improvesound transmission in different habitats, minimiz-ing reverberation and frequency-dependent attenu-ation (Wiley 1991). For instance, pure tonal notesare transmitted better in understorey vegetation,whereas highly modulated sounds or trills transmitbetter in open habitats. In addition, in forestedhabitats, low-pitched sounds are transmitted betterthan high-pitched sounds (Morton 1975, Brown &Handford 1996, Seddon 2005). Finally, low levelsof low-frequency environmental noise in denserhabitats may create a zone where lower frequencysongs should be more common (Ryan & Brenowitz1985, Slabbekoorn & Smith 2002a). Thus, as aresult of different ecological pressures on soundtransmission, inter-population variation is expectedto exist in the acoustic parameters of long-rangesignals due to differences in habitat types (Morton1975, Rothstein & Fleischer 1987, Tubaro & Segu-ra 1994, Brown & Handford 1996). These predic-tions have been collectively grouped under theacoustic adaptation hypothesis (AAH) (Morton1975) and have been studied in a range of taxaincluding insects, anurans, birds and mammals,with variable results (e.g. Dubois & Marten 1984,Tubaro & Segura 1994, Daniel & Blumstein 1998,Slabbekoorn & Smith 2002a, Couldridge & vanStaaden 2004, Blumstein & Turner 2005).

Temporal and acoustic parameters of songs arealso related to individual morphology, such as bodyand beak size (Podos 2001, Podos et al. 2004b,Derryberry 2009). For example, in White-throatedSparrow Zonotrichia albicollis and Swamp SparrowMelospiza georgiana, beak gape is positively corre-lated with song frequency (Westneat et al. 1993),whereas in Darwin’s finches, larger beaks are asso-ciated with narrow frequency bandwidth and lowrates of note emission (Podos 2001). On the otherhand, larger birds produce songs of lowerfrequency (Ryan & Brenowitz 1985). However,although body size is negatively correlated withthe frequency of songs among species (Ryan &Brenowitz 1985, Seddon 2005), little evidencesupports this association in intraspecific compari-sons (Koetz et al. 2007, Cardoso et al. 2008,although see Mager et al. 2007). Thus, morpholog-ical features can be affected by various ecological

pressures in different habitats. For example, billmorphology can change in response to differentfood items, which, in turn, can influence the diver-gence of vocal signals (Podos 2001, Slabbekoorn &Smith 2002b, Seddon 2005).

The majority of vocal recording studies havebeen conducted on oscine passerines (suborder Pas-seri), which are able to learn their songs (Bolhuis& Eda-Fujiwara 2003, Beecher & Brenowitz 2005).In contrast, several studies suggest that suboscinepasserines (suborder Tyranni) have no ability tolearn songs (Kroodsma 1984, Kroodsma & Konishi1991). Current knowledge about the evolution ofacoustic signals in suboscine passerine birds isscarce (Kroodsma 1984, Kroodsma et al. 1987,Lovell & Lein 2004a, 2004b, Seddon 2005) despitethe potential of this group to be a good model sys-tem with which to compare acoustic signals fromdifferent populations. This is because any inter-population song difference in a non-learning spe-cies cannot be attributed to learning biases, thussuggesting local adaptation among populations dueto variation in ecological pressures (see Seddonet al. 2002). The study of a suboscine that displaysinter-population song differences could thereforeprovide insights into how acoustical signalsevolve in response to different selective pressures(Endler 1992, Foster 1999, Boughman 2002, Sed-don 2005). Moreover, acoustical vocal differencesbetween suboscine populations could be useful inhelping to determine their taxonomic status (Isleret al. 1998, 2005).

Suboscines are the dominant group of passerinesin the Neotropics (Irestedt et al. 2001, 2002, Rick-lefs 2002). The Thorn-tailed Rayadito Aphrasturaspinicauda (Furnariidae) is a suboscine endemic tothe temperate austral forests of Chile and Argen-tina, distributed from Fray Jorge National Park(30�S) to the subantarctic forests of the CapeHorn Region (56�S) (Johnson & Goodall 1967,Rozzi 2003, Fig. 1). Three subspecies have beendescribed: A. s. spinicauda, the most widespreadform inhabiting the mainland in Chile and Argentinaand some islands along the Chilean coast, A. s. bull-ocki, which is found only on Mocha Island, and A.s. fulva, restricted to Chiloé Island (Johnson &Goodall 1967, Remsen 2003). The Thorn-tailedRayadito is a small insectivorous non-migratorybird that nests in tree cavities (Vuilleumier 1967,Grigera 1982, Ippi & Trejo 2003, Remsen 2003,see also Moreno et al. 2005, 2007, Van Dongenet al. 2009 for details on reproductive biology).

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Previous records suggest that the species has atleast five different types of vocalizations: a conspic-uous and loud alarm mobbing call, a contact call, astrong and loud trill call, a possible territorialtrilled diurnal song (Ippi 2009) and a dawn trill(C. Estades pers. comm.). Records of previousobservations and information obtained from theliterature were used to define contact and mobbingalarm calls (Vuilleumier 1967, Ippi & Trejo 2003).The wide geographical distribution of the Thorn-tailed Rayadito makes it an appropriate subjectboth to study variation of vocalizations across thespecies range in both connected and isolatedpopulations and to assess how vocal variationvaries in association with morphology and diverseforested habitat structure.

The principal aim of the present study was tocompare vocalizations of populations of Thorn-tailed Rayadito inhabiting different forested habi-tats. Songs of the species have been recorded anddescribed only recently (Ippi 2009). We hypothe-sized that the vocalizations should be differentamong populations and forest types. Predictionsbased on the AAH are that bandwidth of trillsshould be narrower, with lower frequencies and areduced number of notes per trill in more complexand denser forests (i.e. in temperate forests) com-pared with forests with more scattered trees (i.e.subantarctic and sclerophyllous forests) (see Armestoet al. 1996a). In addition, if forest characteristicsaffect acoustic signals transmission: (i) differencesin acoustic variables are expected to occur betweensongs during the breeding and non-breedingseasons, in deciduous forests but not in evergreenforests; and (ii) the same sound (i.e. trill) emittedin two different forest types will degrade differ-ently depending on habitat structure. As differentsubspecies were included in this study, we alsoexplored the relationship between subspeciesclassification and their vocalizations (see Table 1).Finally, and in relation to the effects of morphol-ogy on songs, we expected lower frequencies inpopulations with larger birds, and slower notes pertrill in populations where individuals possessedlonger bills.

METHODS

Recordings of vocalizations of Thorn-tailed Rayadi-tos were made in the austral spring (September–January) in 2006 and 2007 in five different studysites within Chile, spanning a distance of over2400 km from south to north (Fig. 1). Forests atall these sites are classified as southern temperateforest (30–56�S), but there are some importantorganizational and structural differences amongthem, principally a division between subantarctic,temperate and sclerophyllous forest types (Armes-to et al. 1996a). Evergreen temperate rain forests(Chiloé, Mocha and Santa Inés forests) have a largenumber of vegetation strata, high stem density, anda very high biodiversity and biomass of epiphytes(Armesto et al. 1996b, Arroyo et al. 1996). Thesehabitats contrast with the less complex and moreopen subantarctic temperate forests of NavarinoIsland and the disturbed sclerophyllous forest ofManquehue (close to Santiago). Density of treesalso differs among forests. The Santa Inés relict

Figure 1. Geographical distribution of the Thorn-tailed Rayadi-

to Aphrastura spinicauda and the location of the five popula-

tions studied. The distribution map was modified from Jaramillo

(2003) and Rozzi (2003) incorporating our field data (R.A. Vas-

quez unpubl. data).

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Vocalizations of a suboscine bird 791

forest has scattered trees and little understorey(Francois 2004) compared with Chiloé (Aravenaet al. 2002) and Mocha (S. Ippi pers. obs.). There-fore, it is possible to rank the five populations fromlow to high habitat complexity in three categories,while also taking into account the observabledifferences among Santa Inés, Mocha and Chiloéforests (Table 1).

Vocalizations

We were able to differentiate between five types ofvocalizations in Thorn-tailed Rayaditos: (i)mobbing call, (ii) contact call, (iii) loud trill, (iv)repetitive trill and (v) dawn trill (Ippi 2009).Examples of these calls are given in the onlineSupporting Information. Contact calls were

excluded from the present analysis because thesocial context in which they are emitted (familyand ⁄ or flock) made it difficult to identify theindividual(s) that were calling. Dawn trills wereexcluded from inter-population comparisonsbecause individuals were recorded only on ChiloéIsland during November 2009. Both, males andfemales sing all types of calls and songs from (i) to(iv) (Ippi 2009) but no information exists onwhich sexes sing dawn trills.

Vocal recordings were made with a digital recor-der (DAT Sony PCM-M1) and a Sennheiser ME66 microphone, with a sampling rate of 48 kHz.Recordings were made principally during spring(i.e. the breeding season of this species), before1300 h. Additionally, on Navarino and ChiloéIslands we made recordings in autumn and winter

Table 1. Habitat characteristics and subspecies of each of the five populations studied.

Navarino

Island

Chiloe

Island

Mocha

Island

Cerro

Manquehue

Cerro

Sta. Ines

Aphrastura

spinicauda

subspecies

A. s.

spinicauda

A. s. fulva A. s. bullocki A. s. spinicauda A. s. spinicauda

Latitude (�S) 54 41 38 33 32

Longitude (�W) 67 73 73 70 71

Distance to

mainland (km)

1.3–4 2–5 34.2 Mainland

population

Mainland

populationa

Mean annual

temperature (�C)

6 10 12.6 13.9 14.2

Mean annual

precipitation (mm)

450 2097 1373 356 384

Mean annual

humidity (%)

84 82 88 72 83

Type of forest Magellanic

subantartic

Temperate Temperate Sclerophyllous Temperate

(relict)

Seasonality Mixed, mostly

deciduous

Evergreen Evergreen Deciduous Evergreen

Predominant tree

species

Nothofagus pumilio,

N. antarctica,

N. betuloides

Drimis winteri,

N. nitida, Myrtaceous

species

Aextoxicon punctatum,

D. winteri, Luma

apiculata,

Myrceugenia

planipes

Cryptocaria alba A. punctatum,

Myrceugenia

correifolia

Tree density 607–1086 ind ⁄ hab 1075–2160 ind ⁄ ha No information No information 130–1500 ind ⁄ hac

Understorey Low High Medium Almost non-existent Low

Degree of

anthropicogen perturbation

Medium Forest surrounded by

agricultural landscapes

Medium High Medium–high

Complexity classification

(simplest to most complex)

2 3 3 1 3

Information was obtained from the literature (Anderson & Rozzi 2000, Aravena et al. 2002, Carmona et al. 2010, Francois 2004, Gut-

ierrez et al. 2009, Hajek & di Castri 1975, Johnson & Goodall 1967, Lequesne et al. 1999, Perez & Villagran 1985, Willson & Armesto

1996).aCerro Santa Ines is considered a biogeographical island because it is located 60 km from the closest forests and is separated from

them by an arid environment.bA. Gutierrez (unpubl. data).c2270 ind ⁄ ha in Fray Jorge National Park (closest and similar relict forest to Santa Ines) (Gutierrez et al. 2008).

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(the non-breeding season). The methodology usedto detect and record songs and calls of Thorn-tailedRayaditos consisted of one observer walking atconstant speed along different transects or trailsthrough the study site until hearing some vocaliza-tions (no playbacks were used to stimulate birds tosing). We then approached the bird (signal) andstarted recording. Distance between observer andbird varied between c. 5 and 15 m. When makingrecordings at each site, we ensured enough dis-tance between focal individuals to avoid repeatrecordings of the same individuals. Each site wasvisited only once per season. No sex differentiationwas possible during recordings because it is notpossible to sex Thorn-tailed Rayaditos under fieldconditions (Moreno et al. 2005, 2007). Signalacquisition and spectrogram analysis were madewith RAVEN 1.2 software (Cornell BioacousticsLaboratory, Cornell, NY, USA).

Song description

To characterize vocalizations of Rayaditos weadapted a methodology used by several authors(Haavie et al. 2004, Fichtel et al. 2005, Garams-zegi et al. 2005, Seddon 2005), with the followingvariables: (i) minimum frequency, (ii) maximumfrequency, (iii) bandwidth (difference betweenminimum and maximum frequency), (iv) peak fre-quency (frequency in the call or song with themost energy), (v) duration of each trill or note,depending on the type of signal, and (vi) numberof notes per trill or call. Overtones were recordedbut not included in the statistical analyses. A notewas defined as any continuous trace on the sono-gram (sensu Baptista 1977). A trill was defined as aregular pattern of rapidly alternating phases of highand low amplitude for a relatively broad frequencyrange (Slabbekoorn et al. 1999).

Because the four recorded types of vocalizationsdiffer in structure and how they are emitted, wedescribe and analyse each using slightly differentmethods. The mobbing call is a series of repetitivenotes that can last up to several minutes (Ippi2009). For this reason, we selected a period of 3 swith the highest rate of emission of notes per indi-vidual for analyses. For this 3-s sample, we countedthe number of notes per second and recorded theminimum, maximum and peak frequency. Fromboth repetitive and dawn trills, we selected one,two or three consecutive best quality trills perindividual for analysis, based on the clarity of notes

on the spectrogram. When two or three trills wereanalysed, for a given individual, data were averagedto obtain mean values for that individual. Thequality of the trills depended on recordingdistances. The remaining acoustic signal that wasanalysed, the loud trill, was not a repetitive call.Therefore, we analysed it separately with the sameacoustic variables already mentioned, selectingonly one trill per individual.

Sound transmission

To evaluate the differences in degradation of birdsounds in two forest types, we selected a series ofsix trills of Thorn-tailed Rayaditos obtained fromthe commercially available CD ‘Voces de AvesChilenas’ (Unión de Ornitólogos de Chile, Santi-ago, Chile). These trills were broadcasted from aloudspeaker (Sony Mega Bass SRS-A47, Sony Cor-poration, Tokyo) at 1.3 m above the ground insubantarctic forest on Navarino, and in a morecomplex temperate forest on Chiloé. The emittedsounds were then recorded at a distance of 20 mfrom the loudspeaker with the digital recorder andmicrophone mounted at the same height. We rep-licated this standard protocol 10 times in Navarinoand Chiloé (however, we lost one recording inChiloé). Experiments were conducted only duringwindless and sunny days to standardize climaticand ambient noise conditions. We conducted thetrials only at sites where Thorn-tailed Rayaditoswere observed. The point and orientation of the20-m transect were selected at random. In addi-tion, the following habitat features were measuredalong the 20-m transect: number of trees with adiameter at breast height (dbh) > 10 cm, numberof obstacles (i.e. trunks, branches and leaves)between the loudspeaker and microphone, thesum of the length of these obstacles (cm), and acontinuous estimate of canopy cover (%) at eachrecording point. Acoustic variables of the sixrecorded trills were averaged and comparedbetween the Navarino and Chiloé islands.

Morphological measurements

Adult Thorn-tailed Rayaditos were captured inNavarino, Chiloé, Mocha and Cerro Manquehuepopulations. We captured Rayaditos using mist-nets and playback, and ringed each individual witha unique combination of coloured rings and anumbered metal ring (model 1242–3; National

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Band and Tag Co., Newport, KY, USA) under theauthority of Servicio Agrícola y Ganadero (ChileAgricultural and Livestock Service). Morphologicalmeasurements included beak-length (measuredwith callipers to the nearest 0.1 mm), tarsus-length (measured with callipers to the nearest0.1 mm) and weight (measured with a Pesolabalance to the nearest 0.1 g).

Statistical analysis

Statistical analyses were conducted using SPSS forWindows (version 13.0; SPSS Inc., Chicago, IL,USA). Shapiro–Wilks and Levene tests were usedto address normality and variance homogeneity(Sokal & Rohlf 1995). Non-normal variables weretransformed with log, inverse, square-root transfor-mations or a Box-Cox transformation using RUNDOM

BOX-COX freeware (Rundom BC version 1.0, http://pjadw.tripod.com). Differences in acoustic vari-ables of repetitive trills from different populationswere evaluated with a one-way MANOVA. Differ-ences in call structure of repetitive trill, loud trilland alarm calls among forest types and subspecieswere analysed using a linear mixed modellingapproach, incorporating population of origin as arandom factor. Tukey or ANOVA were conducted as aposteriori tests when necessary (Quinn & Keough2002). In the case of alarm calls, Navarino andSanta Inés were excluded from the analysis.

To establish the relationship between the differ-ences in vocalizations and forested habitats fromthe islands Navarino and Chiloé, we carried outthe following analyses, using the data from thesound transmission experiments and habitat struc-ture quantification: (i) to identify the acoustic vari-ables that significantly differ between the twopopulations, we performed a MANOVA (with a post-hoc ANOVA) on the acoustic data from the six trillsthat were broadcast in both Navarino and Chiloé;(ii) to determine the degree to which the sound ofthese trills degrades during propagation, we per-formed a Wilcoxon signed-rank test to assesswhether the emitted and recorded trills differ(Siegel & Castellan 1988); (iii) to identify the habi-tat variables that differed among the sites, weperformed a one-way MANOVA (with a post-hoc ANO-

VA); (iv) to reduce habitat variables, we conducteda non-parametric correlation of the significant vari-ables; and finally, (v) to assess whether habitatcharacteristics could predict the variation observedin acoustic signal transmission, we conducted mul-

tivariate regressions between the habitat variablesselected in (iii) and the acoustic variables selectedin (i). To analyse inter-population differences inbody size we used a MANOVA, including populationof origin and researcher as fixed factors (severalresearchers participated in the captures and mea-surement of Rayaditos). As we were unable to cap-ture any of the birds for which we had songrecordings, we focused on associations betweenmorphological and acoustic variables by comparingmean values of peak frequency and number ofnotes per trill with mean values of weight and bill-length for each population using a Spearman non-parametric correlation coefficient.

Bandwidth is an important variable in predic-tions of the AAH. However, it was highly correlatedwith the maximum frequency of the three vocaliza-tions (repetitive trill: R2 = 0.949, P < 0.001,n = 69; loud trill: R2 = 0.966, P < 0.001, n = 15;and alarm call: R2 = 0.966, P < 0.001, n = 13) andto a lesser degree with the minimum frequency(repetitive trill: R2 = 0.078, P = 0.020, n = 69;loud trill: R2 = 0.140, P = 0.169, n = 15; and alarmcall: R2 = 0.338, P = 0.037, n = 13). Therefore, wedecided to exclude this variable from the MANOVA

and linear mixed model analyses. All valuesreported in the results are means ± SE.

RESULTS

Vocalizations

We recorded a total of 48 h 42 min of Rayaditovocalizations over 40 sampling days, between07:00 and 13:00 h each day. This recording timecorresponded to a total of 100 different individualsfrom which we could obtain 13 alarm calls, 15loud trills, 69 repetitive trills and three dawn trills.

Mobbing call

The mobbing call is a very loud and repetitive sig-nal that is emitted in the presence of a potentialpredator or other threat (Fig. 2a). Mobbing callswere recorded in Cerro Manquehue, Chiloé,Mocha and Navarino. The mean minimum fre-quency of these calls was 2.82 ± 0.21 kHz, maxi-mum frequency was 13.01 ± 0.93 kHz and peakfrequency was 6.02 ± 0.18 kHz, recorded from 13individuals (Fig. 3a). Note rate was rapid, with6.13 ± 0.21 notes per second and the duration ofthis call could last for as long as the predator orthreat was present. Eight of 13 mobbing calls had

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794 S. Ippi et al.

one overtone, two calls had two overtones and noovertones were recorded in three calls. Linearmixed models revealed no significant difference inany mobbing call parameter among the forest types(all P > 0.05).

Loud trill

The loud trill is an acoustic signal that poten-tially has different functions. The trill was heard

(i) when Rayaditos were in the presence of a sud-den threat close to the nest, (ii) when one parentreplaced its partner during incubation, (iii) duringterritorial aggressive interactions and (iv) in thenon-breeding season in response to an unidentifiedstimulus (Fig. 2b). Recordings obtained from 15individuals showed that the duration of this trill wassomewhat variable (mean = 3.22 ± 0.43 s), mini-mum frequency was 1.65 ± 0.12 kHz, maximum

(a)

(b)

(c)

(d)

Figure 2. Representative sonograms of four vocalizations of the Thorn-tailed Rayadito. (a) Mobbing alarm calls from Chiloe Island.

(b) Loud trill from Navarino Island. (c) Repetitive trill from Manquehue. (d) Dawn trill from Chiloe Island.

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frequency was 12.20 ± 0.61 kHz, bandwidth was10.55 ± 0.56 kHz and peak frequency was 4.96 ±0.19 kHz. Mean number of notes per trill was

64.42 ± 8.52. Overtones were recorded in loudtrills, although in variable number: three overtonesin four trills, two in three trills, only one in four

20

Freq

uenc

y (k

Hz)

/Not

es r

ate

Freq

uenc

y (k

Hz)

/Not

es r

ate

Freq

uenc

y (k

Hz)

/Tim

e (s

)

18

16

14

12

10

8

6

4

2

0

18

16

14

12

10

8

6

4

2

0

16

14

12

10

8

6

4

2

0

(a)

(b)

(c)

Figure 3. Acoustic parameters of three vocalizations of Thorn-tailed Rayaditos in different populations. (a) Mobbing alarm calls. (b)

Loud trill. (c) Repetitive trill. Sample sizes for each population are in parentheses. Values indicate mean ± se. * Significant differences

obtained with a post-hoc Tukey test.

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796 S. Ippi et al.

trills, and no overtones in seven trills. Nosignificant differences were detected among thetemperate, sclerophyllous and subantarctic foresttypes (linear mixed models; all P > 0.05; Fig. 3b).

Repetitive trill

Repetitive trills were emitted by both sexes pre-dominately during the breeding season. This trillpossibly has a territorial and ⁄ or mate communica-tion function, as we could frequently hear twoindividuals singing alternately. This trill differedfrom the loud trill because it was shorter and wasemitted over a period of several minutes with reg-ular pauses. Each successive trill was of similarstructure to the preceding one (Fig. 2c) and wasemitted at a rate of 12.34 ± 0.77 trills per minute(range: 4–36, mode = 14.0, n = 57). Trills recordedfrom 69 individuals had a mean duration of 0.63 ±0.01 s with 12.44 ± 0.26 notes per trill. Mean timebetween each trill was 4.85 ± 0.5 s (range 0.98–21.90 s, n = 61). The minimum frequency was2.15 ± 0.05 kHz, maximum frequency was 11.61± 0.38 kHz, bandwidth was 9.46 ± 0.39 kHz andpeak frequency was 4.85 ± 0.04 kHz. Generally,repetitive trills presented one (n = 41), two(n = 13) or three (n = 3) overtones. Twelve of 69trills presented no overtones. Recordings of thistype of song were made at each of the five studysites. Repetitive trills showed significant differencesamong populations (MANOVA F20,199 = 3.52,P < 0.001, n = 69), explained by the difference inpeak frequency between Mocha and NavarinoIslands (Tukey test, P = 0.006) and by the differ-

ence in number of notes per trill between Chiloéand Mocha Islands (Tukey test, P = 0.041; Fig. 3c).Linear mixed models revealed that minimumfrequency, peak frequency and notes per trill alldiffered significantly among subspecies or amongboth subspecies and forest types (Table 2). Mini-mum frequency was lower in A. s. spinicauda com-pared with the other two subspecies (F2,64 = 4.12,P = 0.021; parameter estimates: spinicauda = 0.00± 0.00, bullocki = 0.41 ± 0.17, fulva = 0.59 ± 0.21)and was also lower in the temperate forest(F2,64 = 3.79, P = 0.028; parameter estimates:temperate = 0.00 ± 0.00, sclerophyllous = 0.47 ±0.20, subantarctic = 0.48 ± 0.18). Peak frequencyonly differed among the three subspecies and notamong forest types, and was lowest in bullocki andhighest in fulva (F2,64 = 3.84, P = 0.026; parame-ter estimates: spinicauda = 0.00 ± 0.00, bullocki =)0.19 ± 0.14, fulva = 0.17 ± 0.17). Similarly, notesper trill differed among the three subspecies andwas lowest in bullocki and highest in fulva(F2,64 = 5.43, P = 0.007; parameter estimates: spin-icauda = 0.00 ± 0.00, bullocki = )1.89 ± 0.86, ful-va = 0.47 ± 1.05).

Recordings of repetitive trills were made duringthe non-breeding season (autumn and winter) inNavarino and Chiloé, to allow comparison withthe vocalizations recorded during the breeding sea-son (spring). Trills from the non-breeding seasondid not differ between these populations (MANOVA

F6,18 = 1.70, P = 0.178). In Chiloé, there were nodifferences between seasons (F6,10 = 0.90,P = 0.520). In contrast, in Navarino, there weresignificant differences in the repetitive trillbetween seasons (F5,28 = 5.64, P = 0.001). In thiscase, the minimum frequency was lower in thebreeding season (2.21 ± 0.10 kHz, n = 18) thanduring the non-breeding season (2.66 ± 0.10 kHz,n = 16, F1,32 = 9.58, P = 0.004), whereas themaximum frequency and bandwidth were higherduring the breeding season (12.45 ± 0.56 kHz and10.24 ± 0.56 kHz, respectively) than the non-breeding season (8.84 ± 0.62 kHz, F1,32 = 18.54,P < 0.001 and 6.18 ± 0.66 kHz, F1,32 = 22.51,P < 0.001, respectively).

Dawn trill

Dawn trills were emitted only at dawn, which lastsfor approximately 30 min. They consisted of short(0.29 ± 0.05 s, n = 3) and highly repetitive trills(1.98 ± 0.10 trills per second). Mean minimumand maximum frequency were 1.75 ± 0.13 kHz

Table 2. Descriptive data for three acoustic variables of

repetitive trills in the three different forest types and subspecies

of A. spinicauda.

Subantarctic Valdivian Sclerophyllous n

Minimum frequency (kHz)

spinicauda 2.21 ± 0.13 1.73 ± 1.56 2.19 ± 0.13 35

fulva 2.32 ± 0.15 8

bullocki 2.14 ± 0.08 26

Peak frequency (kHz)

spinicauda 5.03 ± 0.08 4.86 ± 0.13 4.97 ± 0.11 35

fulva 5.03 ± 0.12 8

bullocki 4.68 ± 0.07 26

No. of notes per trill

spinicauda 12.18 ± 0.48 13.41 ± 0.77 13.55 ± 0.64 35

fulva 13.88 ± 0.78 8

bullocki 11.51 ± 0.40 26

n 18 41 10

Values are mean ± se.

ª 2011 The Authors



and 8.85 ± 0.52 kHz (bandwidth 7.10 ±0.64 kHz), whereas peak frequency was 4.63 ±0.80 kHz and the number of syllables 5.78 ± 0.62(Fig. 2d).

Sound transmission

The acoustic variables of the six trills artificiallyemitted were different between sites (MANOVA,F6,12 = 11.41, P < 0.001). Maximum frequency,bandwidth and maximum amplitude were higheron Navarino Island, whereas duration of trill washigher on Chiloé Island (Table 3).

The acoustic variables showed significant varia-tion after transmission across a distance of 20 m,when comparing variables before and after trans-mission, both on Chiloé (Wilcoxon signed ranktest; minimum frequency z = )6.28, P < 0.001;maximum frequency z = )6.28, P < 0.001; band-width z = )6.28, P < 0.001; peak frequencyz = )4.21, P < 0.001; duration of trill z = )4.04,P < 0.001; maximum amplitude z = )6.28, P <0.001) and on Navarino (minimum frequencyz = )6.74, P < 0.001; maximum frequency z =)6.74, P < 0.001; bandwidth z = )6.74, P <0.001; peak frequency z = )4.65, P < 0.001; dura-tion of trill z = )1.06, P = 0.289; maximum ampli-tude z = )6.74, P < 0.001).

The habitats differed between Navarino andChiloé (MANOVA, F4,15 = 12.06, P < 0.001), andunivariate a posteriori tests showed that variablesthat explain differences were: number of treeswith dbh > 10 cm and the number of obstaclesalong a transect (Table 4), although these variableswere correlated (R2 = 0.39, P = 0.003, n = 20).We therefore only used the number of obstaclesalong a transect as a predictor variable to performthe multivariate regression with acoustic variablesthat differed significantly between the populations.A multivariate regression was conducted between

this variable and the acoustic significant variablesfor both populations (F4,14 = 4.74, P = 0.012).Grouping data for both populations, bandwidth(R2 = 0.26, F1,17 = 6.07, P = 0.028, n = 19) andmaximum amplitude (R2 = 0.32, F1,17 = 8.15,P = 0.011) were negatively correlated with thenumber of obstacles, whereas duration of trills(R2 = 0.15, F1,17 = 2.93, P = 0.105) and maximumfrequency were not correlated with habitat fea-tures (R2 = 0.11, F1,17 = 2.04, P = 0.171). Despitethe significant regressions, the proportion of varia-tion in the dependent variables explained by themodel was low, suggesting that other variablesmight also be important in predicting acousticaldegradation of the trills in different habitats.

Morphological differences amongpopulations

Tarsus-length, bill-length and weight of Rayaditosdiffered significantly among populations (MANOVA,F9,316 = 4.49, P < 0.001, n = 145). Bill-length washigher in Cerro Manquehue than in the otherthree populations (Fig. 4a), whereas tarsus-lengthand weight were largest on Mocha Island andsmallest on Chiloé Island (Fig. 4b,c). Although sig-nificant differences were found in the morphologi-cal data measured by different field researchers(F18,368 = 2.80, P < 0.001), no interaction amongpopulations and researchers existed (F9,316 = 1.47,P = 0.158). Weight and tarsus-length were highlycorrelated (R2 = 0.23, P < 0.001, n = 145) andtherefore we used only weight as an estimate ofbody size. Mean population weight values werenegatively related with mean population peak fre-quency (Spearman’s r = )0.63, P = 0.368, n = 4)and mean number of notes per trill was positivelyassociated with mean beak-length (Spearman’sr = 0.60, P = 0.400), although these correlationswere not statistically significant.

Table 3. Acoustic and temporal data from original and recorded trills artificially emitted in Chiloe and Navarino Islands and statistics of

post-hoc univariate tests for differences between both populations.

Original trill (6) Chiloe (9) Navarino (10) F1,17 P

Minimum frequency (kHz) 1.71 ± 0.06 2.32 ± 0.06 2.26 ± 0.5 0.58 0.457

Maximum frequency (kHz) 18.61 ± 0.04 5.93 ± 0.85 8.06 ± 0.48 4.99 0.039

Bandwidth (kHz) 16.91 ± 0.05 3.61 ± 0.87 5.79 ± 0.47 13.56 0.002

Peak frequency (kHz) 4.48 ± 0.04 4.33 ± 0.07 4.27 ± 0.08 0.38 0.545

Duration of trill (s) 0.78 ± 0.01 0.82 ± 0.02 0.78 ± 0.002 6.54 0.020

Maximum amplitude 24686.50 ± 237.25 3324.66 ± 438.1 6287.95 ± 902.12 8.47 0.010

Values are mean ± se and sample sizes are indicated in parentheses.

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798 S. Ippi et al.

DISCUSSION

Vocalizations of the Thorn-tailed Rayadito can bedivided into at least five types: mobbing alarmcalls, contact calls, loud trills, repetitive trills anddawn trills (see also Ippi 2009). Of these, the mob-bing call is probably the most recognizable in thetemperate southern forests of Chile and Argentinabecause this was frequently the first signal we per-ceived when walking through the forest. Nativepeople (Yagans and Mapuches) appreciate Rayadi-tos because, via their mobbing alarm calls, theyprovide warnings about the presence of potentialthreats, such as other people or dogs (Rozzi 2003).Comparisons of each type of vocalization from thefive populations showed that some variation existsin the repetitive trills, although no differences werefound among loud trills and alarm calls. The AAHcan be used to explain some of these differences,although other factors such as morphology alsoseem to be relevant.

The most closely related species to the Thorn-tailed Rayadito is the endangered Masafuera Raya-dito Aphrastura masafuerae, which is the onlyother species in the genus Aphrastura and whichinhabits the oceanic island Alejandro Selkirk (33�S,80�W), 670 km west of the Chilean coast. Accord-ing to Hahn and Mattes (2000), the MasafueraRayadito has three types of acoustic signals: alarmcall, common call and song. Alarm calls were char-acterized by a uniform sequence that can last morethan 10 min, similar to the alarm mobbing calls ofthe Thorn-tailed Rayadito. Both species producethis call in the presence of a predatory threat.However, in the Thorn-tailed Rayadito, behaviourassociated with these calls includes stereotypedmovements that correspond to mobbing behaviour(Curio et al. 1978, Caro 2005, Ippi 2009). Thealarm calls of the Masafuera Rayadito lie between1.8 and 7.6 kHz, with 15.2 syllables per second onaverage, showing somewhat lower but overlappingfrequencies, narrower bandwidth and more notes

Table 4. Habitat data recorded in Chiloe and Navarino Islands along the 20-m transects, and post-hoc univariate tests.

Chiloe (10) Navarino (10) F1,18 P

Canopy cover (%) 60.50 ± 7.24 58.70 ± 10.73 0.01 0.946

No. of trees with dbh > 10 cm 6.30 ± 1.93 0.70 ± 0.26 14.41 0.001

No. of obstacles 43.70 ± 6.90 7.30 ± 2.08 37.10 < 0.001

Length of obstacles (cm) 46.04 ± 7.19 31.46 ± 10.57 1.30 0.269

Values are mean ± se and sample sizes are indicated in parentheses.

(a)

(b)

(c)

Figure 4. Comparison of bill-length (a), tarsus-length (b) and

weight (c) of Thorn-tailed Rayaditos sampled from four sites.

Values indicate mean ± se and sample sizes are in parenthe-

ses. Different letters indicate significant differences among

populations obtained with a post-hoc Tukey test.

ª 2011 The Authors



per second compared with the Thorn-tailed Raya-dito (Fig. 2a). Common calls of the MasafueraRayadito, on the other hand, are similar to theThorn-tailed Rayadito repetitive trill, produced byboth males and females, with regular pausesbetween each trill. However, Masafuera Rayaditocommon calls are longer (1.06 s with pauses of2.1 s) with a narrower bandwidth (3–6 kHz) andare more rapidly modulated (14–17 notes per trill)than the Thorn-tailed Rayadito repetitive trills,although all variables overlapped. Nevertheless,other behaviours associated with this call in theMasafuera Rayadito are similar to that observed inthe Thorn-tailed Rayadito, such as searching forfood or moving between branches. Because weheard Thorn-tailed Rayaditos singing repetitivetrills more frequently in the breeding season, wesuggest that their function is territorial and ⁄ orlong-range mate communication, and they are pos-sibly sung in intersexual duets. The dawn trill is asignal similar to that described for the MasafueraRayadito, because it was emitted during the dawnperiod and had a similar structure, although wecould not determine the sex of the singers. Inter-estingly, some similarities can be observed betweenthe singing behaviour of Thorn-tailed Rayaditosand the oscine Chipping Sparrow Spizella passeri-na. Males of the latter species sing a short and rap-idly delivered trill at dawn. This trill changes aftersunrise, by increasing in duration and inter-songinterval, remaining acoustically similar (Liu & Kro-odsma 2007). The dawn chorus of Chipping Spar-rows functions in close-range communicationamong neighbouring males, while songs sung aftersunrise function as mating calls (Liu & Kroodsma2007). Although the specific functions of Thorn-tailed Rayaditos’ songs are as yet unknown, theseexamples reveal that birds with simple songs canmodify their songs to deal with different social sit-uations (Liu & Kroodsma 2007) and also use thesame song or call to communicate in different con-texts (Marler 2004). Finally, loud trills, which arecommon in Thorn-tailed Rayaditos, have not beendescribed for the Masafuera Rayadito.

Acoustic signals can be affected by morphologi-cal characteristics that influence sound production(Westneat et al. 1993, Podos 2001, Podos et al.2004b), and habitat structure that influences soundtransmission (Morton 1975, Wiley & Richards1978, Richards & Wiley 1980), in oscines as wellas in suboscines (Seddon 2005, Derryberry 2009).Our data provide some insight into the relation-

ship between call structure, habitat and morphol-ogy in a suboscine bird. Repetitive trills weredifferent among populations and ⁄ or forest types,with three acoustic variables showing significantvariation across all the comparisons: the minimumand peak frequency and the number of notes pertrill. Firstly, in terms of sound production, no rela-tionship was found between morphology andvocalization structure. However, although not sig-nificant, the peak frequencies of repetitive trillswere negatively associated with body size across allthe studied populations (see e.g. Ryan & Brenowitz1985, Podos 2001) and the number of notes pertrill was slightly positive associated with beak-length. However, beak-length was not differentbetween Chiloé and Mocha Islands despite thelower notes per trill observed in Mocha comparedwith Chiloé. Beak-length may in itself not be a var-iable that modifies the acoustic characteristics ofsongs (e.g. Podos & Nowicki 2004, Seddon 2005).However, the kinematics of cranial and beak move-ments and ⁄ or beak gape could be more importantin modifying the vocal tract, and therefore the fre-quency and note rates of songs (Westneat et al.1993, Slabbekoorn & Smith 2000, Podos 2001,Podos et al. 2004b, Christensen & Kleindorfer2009, but see Derryberry 2009). Secondly, interms of sound transmission, the Thorn-tailedRayadito vocalizations compared in this studycame from five different populations, including atleast three different types of forests (see Armestoet al. 1996a). We estimated that temperate forestsare more complex and denser than subantarcticand ⁄ or sclerophyllous forests (see Table 1). Mini-mum and peak frequency of repetitive trills fromthe temperate forests were lower than subantarcticforest, which is in accordance with the idea thathigher frequencies are better transmitted in moreopen habitats. When we considered vocal differ-ences across populations, we also found that thenumber of notes per trill was higher in Chiloé thanin Mocha Island. This difference could not beexplained by the AAH, because although some dif-ferences do exist, temperate forest dominates bothislands. Moreover, we failed to find differences inbeak-length between those populations. However,different subspecies of Thorn-tailed Rayadito inha-bit Mocha and Chiloé Islands, which were origi-nally classified based on differences in plumagecoloration (Johnson & Goodall 1967, Remsen2003) and which were also recently confirmed bygenetic evidence (Gonzalez & Wink 2010). In

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800 S. Ippi et al.

addition, acoustic differences were found betweenthe subspecies bullocki and fulva and betweenbullocki and spinicauda. Hence, acoustical differ-ences support the hypothesis that some geneticdifferences exist among subspecies, possibly relatedto isolation during Pleistocene glaciation events(Gonzalez & Wink 2010). From a genetic perspec-tive, differences may be being eroded due to highlevels of gene flow among some populations(Gonzalez & Wink 2010). In other suboscine fami-lies, the number of notes per trill also varies incontradiction to predictions made by the AAH(Seddon 2005). Trills and other signals with highnote repetition rates are subject to degradation byreverberation (Naguib 2003), and for that reason,it is expected that they would be used more inopen than in closed habitats (Richards & Wiley1980, Slabbekoorn & Smith 2002a). Moreover, ourresults showed that the same sound (i.e. repetitivetrill) emitted in two different forest types (Chiloéand Navarino) suffered modifications in acousticvariables including maximum frequency, band-width, sound duration and maximum amplitude.As predicted by the AAH, higher frequencies wereaffected to a greater degree because their energy islost through reflections in branches and leaves(Morton 1975). Further, the energy recorded washigher in Navarino where forests are less complex.However, longer trills were recorded in Chiloéthan Navarino, and although this result is more dif-ficult to explain, reverberations and echoes couldhave slightly extended them, counteracting theattenuation in a more complex habitat. This pat-tern has previously been reported for narrow-fre-quency bandwidth notes (Slabbekoorn et al. 2002).Our transmission experiments were conducted at aheight of 1.3 m and Thorn-tailed Rayaditos oftensing at much greater heights, where the habitatstructure could be somewhat different from nearthe forest floor. However, we assumed that habitatstructure at different heights would be correlatedand thus our measurements at 1.3 m height wouldbe a good estimate of degradation and attenuationof songs in this inter-population comparative study.Therefore, acoustical signal transmission is affecteddifferently in Navarino and Chiloé, and thus songsand long-range acoustic signals would be suscepti-ble to changes that can improve the signal trans-mission. In support of the AAH, we found thatthe maximum frequency (and consequently thebandwidth) had a tendency to be lower in temper-ate than in subantarctic and sclerophyllous forests,

for both the repetitive trills and the alarm calls,although these differences were not significantlydifferent. Finally, our results showed that the num-ber of notes per second in mobbing the alarm callswas higher in sclerophyllous than temperate for-ests, also in accordance with the AAH.

Overall, our results suggest that only one vocali-zation type showed geographical variation, in threeacoustical variables, which can be affected by habi-tat structure. In addition, morphology may also beinfluencing these differences. Furthermore, isola-tion of the studied populations would contributeto these differences, if gene flow is limited by dis-tance and ⁄ or other barriers. The Thorn-tailedRayadito is a suboscine species, and the divergencein its vocalizations would not involve learning pro-cesses, but are more likely due to genetic differen-tiation or plasticity. However, low sample sizes,particularly in loud trills and mobbing alarm calls,could have reduced the power of detecting statisti-cal differences among populations, forest typesand ⁄ or subspecies.

It is possible that the differences in forest typesstudied here are not a strong enough selectiveforce to change all the acoustic variables of trills ofThorn-tailed Rayaditos. This could occur becauseThorn-tailed Rayaditos normally sing repetitivetrills closer to the canopy (and not at ground level)and thus frequency attenuation could be similar indifferent places. However, Thorn-tailed Rayaditosalso feed along forest edges and in shrubland habi-tats, which may partially explain why the peakfrequency of repetitive trills in this species(4.85 kHz) is more similar to bird songs of tropicalpasserine species inhabiting forest edges (3.6 kHzfor suboscines and 4.7 kHz for oscines) thanupper-forest bird songs (3.1 kHz), although thesevalues could be biased by body size and phylogeny(Morton 1975, Ryan & Brenowitz 1985). Finally,Thorn-tailed Rayadito trills from Chiloé have thesame acoustic characteristics in the breeding andthe non-breeding season. This pattern followed ourpredictions, as the evergreen forest does notchange seasonally. However, contrary to the pre-dictions of the AAH, trills from Navarino madeduring the breeding season (denser habitat due tothe presence of foliage) had a higher maximumfrequency than during the non-breeding season(more open habitat).

Although the inter-population differences invocalization structure did not completely corrobo-rate previous subspecies divisions (Johnson & Goo-

ª 2011 The Authors



dall 1967), bullocki did differ from the other twosubspecies spinicauda and fulva. Isolation of MochaIsland populations would be higher due to greaterdistance between the island and the continent, pos-sibly restricting gene flow. Gonzalez and Wink(2010) suggested that genetic differences betweenMocha Island and the mainland could be related toits status as a palaeorefuge during the last Pleisto-cene glacial events. In support of Gonzalez andWink (2010) our results also suggest that somegenetic differences might exist because songs andcalls are not learned in suboscine birds and henceare not influenced by cultural or social influences(Kroodsma 1984, Kroodsma & Konishi 1991).However, we suggest that genetic differencesresulting from different ecological pressures,genetic drift and ⁄ or limited population gene flowwould suggest that these taxa are in the earlystages of divergence, mainly due to a relativelyshort history of isolation and ⁄ or limited extent ofgeographical isolation, particularly among main-land populations. If isolation were reinforced, forexample by aridification of sclerophyllous shrub-lands, gene flow would be weakened and subspe-cies differences may become more pronounced. Inany case, more detailed experiments are needed todetermine the influence of habitat type on songsand calls in the Thorn-tailed Rayadito and othersuboscines, if we are to disentangle how selectiveforces interact with other traits, such as body andbeak size. Therefore, although our results are notconclusive, we have shown that acoustic signals,jointly with coloration and body size (Johnson &Goodall 1967, present study, R.A. Vásquez et al.unpubl. data), may express a certain degree ofgenetic differentiation among isolated and ⁄ ordistant populations.

We are especially grateful to Cristóbal Venegas, IvaniaCotorás, Paula Marín and Verónica Quirici for their fieldsupport provided during this study, Claudia Cecchi andAlvaro Rivera for their assistance with acoustic andstatistical analyses, and Álvaro Gutiérrez for his usefulcomments about characterization of forest types ofChilean temperate forest. Two anonymous reviewersimproved considerably a previous version of this manu-script. Enrique Ippi helped with figures and made thedistribution map of the Rayadito. Granja Educativa Man-quehue, Fundo Los Cisnes and Mario Hahn from MochaIsland kindly allowed us to conduct fieldwork on theirproperties. Research was funded by FONDECYTs1060186 and 1090794, ICM-P05-002, PFB-23 CONI-CYT-Chile to R.A.V., and a CONICYT-Chile graduate

fellowship AT 24060066 to S.I. This paper is a contribu-tion to the research activities of the Omora Ethnobotani-cal Park (http://www.omora.org) and Senda DarwinBiological Station (http://www.sendadarwin.cl), mem-bers of the Chilean Network of Long-Term Socio-Eco-logical Study Sites, financed by the Institute of Ecologyand Biodiversity. Research was conducted under permitNo. 5193 issued by the Servicio Agrícola y Ganadero,Chile, with the supervision of the Ethics Committee ofthe Faculty of Sciences, Universidad de Chile.

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Received 11 September 2010;revision accepted 28 July 2011.Associate Editor: Ian Hartley.

SUPPORTING INFORMATION

Additional Supporting Information may be foundin the online version of this article.

Data S1. Five types of vocalizations in Thorn-tailed Rayaditos.

Please note: Wiley-Blackwell are not responsiblefor the content or functionality of any supportingmaterials supplied by the authors. Any queries(other than missing materials) should be directedto the corresponding author for the article.

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