Journal of The e€ects of fragmentation on ¯uctuating asymmetry Applied Ecology 2000, 37, in passerine birds of Brazilian tropical forests 1013±1028 M. ANCIAÄ ES*{ and M.Aà .MARINI{ *PoÂs-GraduacËaÄo em Ecologia, ConservacËaÄo e Manejo da Vida Silvestre, ICB, CP 486, Universidade Federal de Minas Gerais, 30161±970, Belo Horizonte, MG, Brazil; {Natural History Museum and Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045±2454, USA; and {Departamento de Biologia Geral, ICB, CP 486, Universidade Federal de Minas Gerais, 30161±970, Belo Horizonte, MG, Brazil

Summary 1. Fluctuating asymmetry (FA) refers to the di€erence between the right and left sides in characters that should otherwise be bilaterally symmetrical, but whose expression is a€ected by epigenetic stress during development. Forest fragmenta- tion may promote an increase in FA in isolated populations, by either genetic or environmental stress. FA may function as a biomonitor index in conservation biol- ogy if increased levels were observed in populations from fragmented habitats. 2. We tested the hypothesis that FA is higher in birds from small tropical forest patches than in large forest tracts. We measured wing and tarsus FA on mist-netted birds from seven fragments and seven continuous areas from south-eastern Atlantic rain forest in Brazil. We performed FA comparisons between fragments and con- trol groups for the whole community, for individual foraging guilds and for the six most abundant species. 3. Wing and tarsus FA were signi®cantly greater in fragments than continuous areas for the whole community and were both negatively correlated with forest fragment size. Di€erences in FA varied among foraging guilds, being more evident for insectivorous species, especially those feeding in or near the understorey. 4. FA levels increased signi®cantly in forest fragments in at least one trait for ®ve of the six most abundant species. There was no correlation between tarsus and wing asymmetries for the individuals of any species nor any di€erence between the degree of asymmetries of these characters. 5. We suggest that FA is a useful tool to assess the e€ects of fragmentation on for- est birds, and may be applied in monitoring neotropical birds. FA indices might be pro®tably developed, particularly in species most threatened by fragmentation e€ects and when investigated in di€erent morphological characters.

Key-words: conservation, deforestation, developmental stability, habitat distur- bance, neotropical birds. Journal of Applied Ecology (2000) 37, 1013±1028

Introduction The e€ect of fragmentation on neotropical bird communities has been investigated in some depth Habitat fragmentation is a major cause of species or (Willis 1979; Terborgh & Winter 1980; Lovejoy et al. population extinctions. It may interrupt gene ¯ow, 1984, 1986). Sha€er (1990) reviewed the inverse rela- a€ect population size and promote inbreeding tionship between forest size and species richness, (Wayne et al. 1992). Anthropogenic disturbances to illustrating the use of island biogeography theory to natural habitats create the need for methods to the design of natural reserves. Other studies have monitor the size and quality of wildlife populations. shown that forest clearance a€ects both habitat selection and movements of birds (Simberlo€ 1995; Wiens 1995), decreases food supplies and nest site Correspondence: Marina Anciaes, Natural History Ä availability (Rappole & Morton 1985; Burke & Nol Museum, Division of Ornithology, Dyche Hall, University # 2000 British of Kansas, Lawrence, KS 66045±2454, USA (fax 785 864 1998), and increases nest predation and parasitism Ecological Society 5335; [email protected]). (Robinson 1989). Bierregaard & Lovejoy (1989) 1014 showed that bird abundance decreased in Amazo- diversity (Brawn et al. 1998). We compared FA in Fluctuating nian fragments after isolation, where insectivorous the wing and tarsus of passerines from forest frag- asymmetry in species from the understorey were most a€ected. ments and large tracts of continuous Brazilian birds Although many studies have focused on distur- Atlantic Forest. We searched for di€erences among bances to neotropical bird communities in response foraging guilds in FA alteration, aiming to evaluate to deforestation, there are few studies that evaluate its potential application as a tool for monitoring whether fragmentation also promotes alterations in neotropical birds. avian morphology. Fluctuating asymmetry (FA) may be used for monitoring genetic and environmental stress su€ered by natural populations (Leary & Allendorf 1989; Materials and methods Parsons 1992; Sarre, Dearn & Georges 1994). FA re¯ects disturbances during the development of S T U D Y S I T E S A N D B I R D C A P T U R E S characters that a€ect an organism's ability to develop uniform traits (developmental stability) The research was conducted in seven large control (Soule 1967; Wayne, Modi & O'Brien 1986; Palmer areas and seven forest fragments, all within the Bra- 1994). One possible scenario is that the loss of zilian Atlantic Forest biome (Fig. 1 and Table 1). genetic variability in isolated populations may result The vegetation of the areas sampled was classi®ed in decreased developmental stability and increased as either `dense tropical rain forest' or `semi-decid- levels of FA (Parsons 1990; Clarke 1992; Sherry & uous dry tropical forest' according to the Brazilian Lord 1996). High levels of morphological alteration Institute of Geography and Statistics (IBGE 1988). and FA have been observed where heterozygosity Control areas were characterized as continuous for- has been depressed (Hutchison & Cheverud 1995). est tracts larger than 2000 ha, and fragmented for- The African cheetah Acinonyx jubatus, for example, ests were represented by areas of up to 350 ha that has very low genetic variation due to population had been isolated, by a distance of at least 3000 m bottlenecks and apparently has higher FA than from other forests (see exceptions below), for at other big cats (Wayne, Modi & O'Brien 1986). least 20 years. Other disturbances also increase levels of FA. Each locality was sampled once during 4±8 conse- Greater indices of FA have been observed in ®sh cutive days, in order to measure at least 60 indivi- from areas highly polluted with DDT (Valentine & duals. Field work took place in July 1996, between Soule 1973) or mercury (Ames, Felley & Smith April and October 1997, and between February and 1979), and in cell patterns of damsel¯y wings April 1998 (Table 1). Sampling was conducted dur- exposed to the insecticide carbaryl (Hardersen, ing these periods in order to avoid birds in moult, Wratten & Frampton 1999). It has also been sug- which most commonly occurs between November gested that nutritional stress increases FA in and March (Sick 1993). The sample size was aimed humans (Perzigian 1977). Sarre (1996) concluded to maximize statistical power and test FA as an that environmental modi®cation caused by habitat index based on a reasonably low sample e€ort. destruction was severe enough to increase the devel- Rates of individual and species capture usually sta- opmental instability and FA in Australian lizards. bilized only after 5 days. Because genetic and environmental stress have a Two areas were excluded from community ana- cumulative e€ect, FA may represent a sensitive bio- lyses (Table 1) because of their low sample sizes logical indicator of environmental stress in popula- after 8 sampling days. Two fragments had an uncer- tions under genetic stress (Clarke 1992; Parsons tain isolation distance of approximately 500 m. In 1992). Sarre, Dearn & Georges (1994) suggest that spite of the scarce literature about the dispersal abil- FA re¯ects individual ®tness better than life tables, ity of forest birds, we included them as fragments and thus FA may be of value in biological monitor- because of their area and time since deforestation ing programmes. Recent studies have demonstrated events in those regions. However, we could not con- that fragmentation a€ects the natural levels of FA. ®rm that birds were isolated in these two areas. His- Lizards from small habitat patches present higher torical and topographical information about the levels of FA than those from large ones (Sarre & study sites was obtained from those institutions that Dearn 1991; Sarre 1996). Squirrels become slightly gave permission for the ®eld work (FundacË aÄ o SOS more asymmetrical in woodland fragments (Wauters Mata Atlaà ntica, SaÄ o Paulo, SP; FundacË aÄ o J.P. de et al. 1996), and Lens et al. (1999) observed Oliveira, Campinas, SP; Instituto Florestal do increased FA in more degraded remnants of afro- estado de SaÄ o Paulo; Companhia de Saneamento de tropical forest for seven bird species. The Brazilian Minas Gerais e Instituto Ambiental do Parana ), in # 2000 British Atlantic Forest has been greatly deforested in spite the form of satellite imagery, aerial photographs Ecological Society of its high species richness and endemism level (Fon- and topographic maps from the forests. Maps from Journal of Applied Ecology, 37, seca 1985; Ha€er 1990), being considered a main IBGE of 1 : 50 000, 1 : 100 000 and 1 : 250 000 scales 1013±1028 priority for the conservation of neotropical bird were also consulted. 1015 M. AnciaÄes & M.AÃ. Marini N

South America

50° 44°

GO MG R. Paranaiba

R. Grande R.Doce 20° R. São Francisco F2 ES R. TietéSP C3

CI C6 RJ R. Paraná R. Paranapanema F4 R. ParaibaC2 do Sul F6 FI F5 F7 F3 C7

25° R. RibeiraC4 C5 PR

Large forest Fragment

State boundary 0 200 400 km River

Fig. 1. Geographic location of the control forests and fragments sampled. Detailed information is given in Table 1.

Birds were captured with 36-mm mesh mist-nets E C O L O G I C A L A N D B E H A V I O U R A L G R O U P S (12 m long by 2Á5 m high) opened on linear transects Species were classi®ed according to their degree of in the understorey from 06:30 h in the morning to dependence on the forest for reproduction, main 17:00 h in the afternoon. Each bird was identi®ed foraging habitat and diet. Dependence on forest was to species and received a metallic ring provided by represented by three categories: 1, independent; 2, the Centre for Bird Monitoring, Brazilian Institute semi-dependent; 3, dependent (Silva 1995). The cate- for Environmental A€airs (CEMAVE, IBAMA). gories of foraging strata were de®ned as: T, terres- Nomenclature followed Sick (1993). trial; U, understorey; M, medium; C, canopy (Sick 1993; Stotz et al. 1996). The main diet of each spe- cies was classi®ed as: I, insectivorous; F, frugivor- T Y P E S O F C O M M U N I T Y A N A L Y S I S ous; O, omnivorous; G, granivorous (Sick 1993). The communities were analysed using three di€erent procedures. In the ®rst community analysis, all spe- F A E S T I M A T E S cies present in each area were considered (analysis I). In the second analysis, only species present in Estimates of FA were calculated following the both forest types (control areas and fragments) were method of Palmer & Strobeck (1986) adapted fol- considered, to avoid the e€ect of di€erent species in lowing the suggestions of Sarre & Dearn (1991), the results (analysis II). In the third type, the same Evans, Martins & Haley (1995), Sarre (1996) and species as in analysis II were considered but sample Wauters et al. (1996). Wings and tarsi were mea- # 2000 British sizes of each species were controlled for, in order sured twice in each individual with dial callipers of Ecological Society to avoid the e€ect of di€erences in the abun- 0Á02 mm precision, in order to decrease measure- Journal of Applied Ecology, 37, dance of each species among forest types (analysis ment error. Only one researcher took the measure- 1013±1028 III). ments, with subsequent measurements taken after 1013±1028 Ecology birds asymmetry Fluctuating 101 Journal Ecological # 2000 6 , of British 37 Applied Society , in

Table 1. Characteristics of the study sites: FT, forest type (C ˆ control, F ˆ fragment); Area, approximate forest area in hectares; DCF, minimum distance to the closest forest fragment (m); TSI, approxi- mate time since isolation (years); ALT, altitude (m); n, number of birds measured; Faz., Farm; RPAC, Reserve for Environmental Preservation of Companhia de Saneamento de Minas Gerais; RE, Ecologi- cal Reserve; PE, State Park; RPPN, Private Reserve; PARNA, National Park; EE, Ecological Station. Most sites names and localities are in Caà mara (1991)

Geographical TSI ALT Site Study site Municipality (state) FT coordinates Area (ha) DCF (m) (years) (m) n Sampling period

F1 Faz. V. BencË aÄ o Bananal (SP) F 22410 S 44190 W 15 3000 30 550 89 28 April3 May (1997) F2{ RPAC Tabooes Ibirite (MG) F 20010 S 44030 W 100 500 20 800 80 14 February20 April (1998) F3 RE Santa Genebra Campinas (SP) F 22540 S 47030 W 250 5000 20 500 120 4±6 July (1996) 28±31 July (1997) F4{ Faz. SaÄ o JoaÄ o Souzas (SP) F 22440 S 46540 W 250 500 20 500 67 6±11 August (1997) F5 PE V. R. E.Santo Feà nix (PR) F 23540 S 51580 W 350 3000 50 350 105 14±19 May (1997) F6* Faz. Doralice Jataizinho (PR) F 23160 S 51020 W 150 10 000 30 500 13 18±21 June (1997) F7* Faz. Remansinho IbiporaÄ (PR) F 23150 S 50580 W 350 10 000 30 500 17 21±26 June (1997) C1 RE Ga lia GarcË a (SP) C 22390 S 50240 W 2180 ± ± 600 115 2±4 August (1997) C2 Faz. Retiro Paracambi (RJ) C 22360 S 43420 W 30 000 ± ± 420 90 19±26 April (1997) C3 PE S. Brigadeiro Erva lia (MG) C 20500 S 42390 W 13 000 ± ± 1370 105 1±5 October (1997) C4 RPPN Salto Morato GuaraquecË aba (PR) C 25180 S 48190 W 120 000 ± ± 40 110 1±6 June (1997) C5 PE Marumbi Morretes (PR) C 25280 S 48500 W 150 000 ± ± 480 105 25±30 May (1997) C6 PARNA Itatiaia Itatiaia (RJ) C 22290 S 44330 W 25 000 ± ± 700 107 15±19 July (1997) C7 EE Jure ia Peruõ be (SP) C 24190 S 46590 W 70 000 ± ± 20 103 4±8 July (1997)

*Excluded from the community analysis due to small sample sizes. {Uncertain DCF. 1017 completely closing the callipers. Wing measurements metries of di€erent species can be made. These tests M. AnciaÄes & were taken by ¯attening the wing against a paper- were conducted separately for each area and each M.AÃ. Marini covered clipboard, marking the length of both species with a large sample size. wings, and afterwards measuring them with calli- Measurement error (ME) was estimated through pers. Tarsi were measured from the notch at the both the repeatability of measurements and the sig- back of the tibia±tarsus joint to the distal point ni®cance of FA in relation to ME. We analysed 1±4 obtained by bending the toes to an angle of 90 to species with large sample size (n > 10) in each family the tarsus. Wings with damaged or moulting feath- or subfamily, in control areas. The repeatability of ers, as well as tarsi with anomalies, were not mea- measurements was estimated on each side of each sured. Migratory species and non-passerines were characteristic in a species through one-way analysis not considered. of variance. This approach is described by Sokal & The FA of each character was initially calculated Rohlf (1981) and Lessells & Boag (1987). Palmer &

for each individual (FAi) as: Strobeck (1986) explain that two measurements of each side are enough to considerably reduce the FAi ˆ R L†=‰ R ‡ L†=2Š eqn 1 magnitude of ME, allowing a reliable estimate of where R ˆ mean of right side measurements, and L repeatability of measurements. High repeatability ˆ mean of the left side measurements. values have been observed in some studies (Swaddle This estimate was used for the analysis of the con- & Witter 1994; Mùller 1995a,b; Wauters et al. cordance of the pattern to the ideal FA (normal dis- 1996). In order to attain values as high as possible, tribution and a mean not signi®cantly di€erent from we conducted an evaluation of the best measuring zero). The values used refer to the relative asymme- technique, based on ®ve di€erent measurements on try in order to avoid the e€ect of size variation in wings and two on tarsi, collected during 6 months the characteristic. Except for comparisons of FA for of ®eld work. The gain obtained by using higher the whole community, in subsequent analysis precision callipers (0Á02 mm compared with 0Á05 unsigned asymmetry values were used (Palmer & mm) was also tested prior to collecting data. Strobeck 1986, 1992; Evans, Martins & Haley 1995; A two-way analysis of variance was conducted for Sarre 1996). each selected species to asses the signi®cance of rela- tive FA in relation to ME, following the protocol The parameter of FA for each community (FAc) was estimated for each characteristic as the variance described by Palmer (1994). Individuals were the of the FA estimate described in equation 1: random factor (n ± 1 d.f., n ˆ number of indivi- duals) that assessed variation in size or shape among individual birds, and side (1 d.f.) was the FAc ˆ V R L†=‰ R ‡ L†=2Š: eqn 2 ®xed factor that assessed directional asymmetry. The index based on the variance of relative FA is The individuals±side interaction (n ± 1 d.f.) assessed recommended because it is sensitive to small FA non-directional asymmetry (typically FA) and the variations in cases where there is size variation in error assessed variation in replicate measurements. the characteristic and when directional asymmetry Swaddle, Witter & Cuthill (1994) argue that estimat- and anti-symmetry are absent (Palmer & Strobeck ing the magnitude of measurement error in relation 1986). Statistical analysis based on this index may, to FA is more appropriate than calculating the thus, detect small di€erences among large samples. repeatability for a trait length, in order to evaluate whether variation in estimated asymmetry is signi®- cantly greater than can be accounted for by mea- S T A T I S T I C A L A N A L Y S I S surement error. High repeatability values do not In order to evaluate the concordance between our imply low error relative to asymmetry. data and the `ideal ¯uctuating asymmetry', we deter- Comparisons of FA levels among control areas mined, for each species and community, whether the and fragments were conducted through t-tests and mean values of the relative asymmetry (equation 1) two-way analyses of variance, following Palmer & for each character di€ered signi®cantly from zero Strobeck (1986), Sarre (1996) and Wauters et al. and whether the corresponding frequency distribu- (1996). Tukey tests for unequal sample sizes were tion departed from normality. This was veri®ed used to detect the honest signi®cant di€erence through a one-sample t-test and a Kolmogorov± among samples when the e€ect was signi®cant in the Smirnov (KS) test for known means, respectively two-way analysis of variance (Sokal & Rohlf 1981). (Sokal & Rohlf 1981). Di€erences of relative FA levels between commu- Linear regressions of individual unsigned relative nities from large contiguous forests and forest frag- asymmetry, against individual mean trait size, were ments were tested estimating a relative FA index for # 2000 British used to test the linear dependency of the asymmetry each community (equation 2) and then running a t- Ecological Society on character size, following Evans, Martins & Haley test to compare the means from each forest type. Journal of Applied Ecology, 37, (1995) and Dufour & Weatherhead (1996). This ana- Each species with a large sample size was analysed 1013±1028 lysis is necessary before comparisons among asym- based on the individual's relative FA levels on large 1018 forests and fragments, through a t-test with indivi- both characters for all the 18 species, as veri®ed Fluctuating duals as sampling units, instead of communities. through the signi®cance of the F-values for the indi- asymmetry in Analysis of diet and foraging strata in¯uences on vidual±side interaction in the analysis of variance birds relative FA levels were conducted entering each indi- (Table 2). vidual bird as an independent datum. Small sample sizes and missing values precluded analysis by mean F R A G M E N T A T I O N E F F E C T S values on each species or running only a single ana- lysis of variance. The relative FA of both wings and tarsi was larger The relationship between relative FA in each in forest fragments than in control forests within the characteristic and forest size was achieved through Atlantic Forest for all three types of community the Pearson correlation coecient. We conducted comparisons. Fragmentation e€ects were thus evi- linear regressions of the unsigned relative FA in dent when communities were controlled for species wing and tarsus on each community (equation 2), and sample sizes (Fig. 2 and Table 3). Wing and tar- from the analysis I, against the logarithm of the cor- sus asymmetries were both negatively correlated responding forest area (Sokal & Rohlf 1981). The with forest size (wing: r ˆ 0Á72, P ˆ 0Á04, tarsus: r correlation between wing and tarsus asymmetries ˆ 0Á83, P ˆ 0Á01) (Fig. 3). was tested for each species with large sample size, Relative FA varied among control forests and following Evans, Martins & Haley (1995). Relative fragments independently of foraging habitat for asymmetries for each character were plotted, with wings, but not tarsi. There was a signi®cant e€ect of each point representing one individual, and a linear fragmentation and foraging strata only on relative regression analysis was performed using the Pearson tarsi FA. Tarsi FA was higher in fragments for spe- correlation coecient. cies foraging from the terrestrial strata to the under- storey and also for those foraging from the understorey to the medium strata. The variation of Results relative FA on wings and tarsi between control for- We measured 1236 individuals from 100 passerine ests and fragments depended on the diet of the spe- species in the 14 areas, in a total sampling e€ort of cies. Relative FA on wings was higher in fragments 8093 net hours. The communities comprised than in control forests for insectivorous species, between 19 (F4) and 37 species (C4) and the number whereas on tarsi it was higher for both insectivorous of individuals sampled in each area varied from 67 and omnivorous species (Table 4). There was no to 120, excepting the areas excluded from commu- interaction of relative FA on wings and tarsi for nity analysis (Table 1 and Appendix 1). Net capture combined groups of foraging strata and diet, among rates varied from 2Á81 (F3) to 8Á87 (C4) species per control forests and fragments (Table 5). 100 net hours among the communities. Only six bird species presented large enough sam- All communities and species exhibited relative FA ple sizes (n > 10) in each forest type to be compared on wings and tarsi of individuals. The asymmetry separately. Di€erences in relative FA in characters values for wings and tarsi for individual birds were between control forests and fragments were variable normally distributed (all KS-d > 0Á05, P > 0Á10) among species. Conopophaga lineata exhibited di€er- with means equalling zero (all t > 0Á08, P > 0Á09) in ences in relative FA levels between control forests all the analysed cases. and fragments only for wings; Dysithamnus mentalis, The relative asymmetry values for wings and tarsi Turdus albicollis and Trichothraupis melanops only of each individual were independent of the mean for tarsi; Platyrinchus mystaceus for both characters; character size in all communities and species (all r and Tachyphonus coronatus did not show di€erences < 0Á241, P > 0Á078). There were, however, two in either character (Table 6). All species presented exceptions: the Pearson correlation coecient was similar levels of relative FA between wings and tarsi signi®cant for tarsi in one community (r ˆ 0Á06, P ˆ in control forests or in fragments, and relative FA 0Á01), but its value was too low and thus did not in wings was not correlated with relative FA on indicate that a considerable proportion of the var- tarsi in any species (Table 6). iance in character relative asymmetry was explained by mean character size; and results for Dysithamnus Discussion mentalis indicated that a high proportion of the var- iance in tarsus relative asymmetry was explained by A higher mean level of relative FA in birds' wings mean tarsus size, although not signi®cantly (r ˆ and tarsi was found in the forest fragments of the 0Á94, P ˆ 0Á32). Brazilian Atlantic Forest. This suggests that passer- All wings and tarsi in the 18 species selected for ine communities exhibit morphological alterations, # 2000 British measurement error analysis (see Appendix 1) expressed as asymmetry, due to habitat fragmenta- Ecological Society showed a high measurement repeatability (all r > tion. Sarre & Dearn (1991) found a negative correla- Journal of Applied Ecology, 37, 0Á94) for both right and left sides. Relative FA was tion between FA in lizards and island size, which, in 1013±1028 signi®cantly higher than the measurement error in accordance with our results, demonstrates that FA 2 2 1019 Table 2. The analysis of variance (mean squares, MS, component of variance  10 ± s I S, and F-values) of wing (W) and M. AnciaÄes & tarsus (T) measurements for 18 species. Percentage contribution for error (replicate measurement variation) relative to the à interaction of individuals  side (I  S) source of variation (relative ¯uctuating asymmetry) in all species for both characters M.A. Marini are also given. **All tests were signi®cant at P < 0Á01

I Â S Error FA-error Species Trait 2 d.f. MS** d.f. MS F** s IÂ S E/FA (%)

Dendrocincla turdina W 37 1Á18 76 0Á01 92Á93 58Á28 2Á18 T 38 0Á02 78 0Á00 10Á40 0Á85 21Á28 Lepidocolaptes fuscus W 32 0Á63 66 0Á01 47Á90 30Á89 4Á26 T 33 0Á19 68 0Á00 74Á84 9Á23 2Á71 Philydor atricapillus W 25 1Á35 52 0Á00 819Á10 67Á49 0Á24 T 25 0Á02 52 0Á00 10Á40 0Á79 21Á28 Automolus leucophthalmus W 12 1Á98 26 0Á01 173Á00 98Á21 1Á16 T 13 0Á02 28 0Á00 18Á08 1Á15 11Á71 Dysithamnus mentalis W 13 0Á35 28 0Á00 508Á79 17Á27 0Á39 T 15 0Á03 32 0Á00 63Á11 1Á61 3Á22 Pyriglena leucoptera W 27 0Á87 56 0Á00 295Á54 43Á30 0Á68 T 30 0Á04 62 0Á00 40Á24 1Á94 5Á10 Conopophaga lineata W 12 0Á22 26 0Á01 24Á26 10Á45 8Á60 T 13 0Á02 28 0Á00 37Á43 1Á14 5Á49 Platyrinchus mystaceus W 30 0Á43 62 0Á01 90Á18 21Á00 2Á24 T 32 0Á09 66 0Á00 46Á45 4Á55 4Á40 Chiroxiphia caudata W 38 0Á55 78 0Á01 107Á75 27Á38 1Á87 T 38 0Á06 78 0Á00 28Á18 2Á99 7Á36 Ilicura militaris W 14 0Á68 30 0Á00 170Á44 33Á55 1Á18 T 16 0Á05 34 0Á00 42Á51 2Á53 4Á82 Platycichla ¯avipes W 13 1Á36 28 0Á00 2822Á46 67Á72 0Á07 T 13 0Á03 28 0Á00 70Á82 1Á68 2Á87 Turdus albicollis W 49 1Á62 100 0Á03 64Á84 79Á77 3Á13 T 50 0Á06 102 0Á01 8Á041 2Á73 28Á40 Basileuterus culicivorus W 28 0Á34 58 0Á00 135Á99 17Á01 1Á48 T 28 0Á04 58 0Á00 21Á85 1Á84 9Á59 Tachyphonus coronatus W 21 0Á40 44 0Á00 166Á58 19Á62 1Á21 T 20 0Á06 42 0Á00 96Á53 3Á17 2Á09 Trichothraupis melanops W 84 0Á74 170 0Á01 52Á38 36Á38 3Á89 T 84 0Á03 170 0Á00 12Á72 1Á32 17Á07 Habia rubica W 31 0Á55 64 0Á01 41Á35 26Á98 4Á96 T 31 0Á05 64 0Á00 19Á95 2Á41 10Á56 Tangara seledon W 11 0Á30 24 0Á00 106Á92 14Á93 1Á89 T 11 0Á08 24 0Á00 49Á92 3Á88 4Á09 Haplospiza unicolor W 18 0Á60 38 0Á03 23Á68 28Á94 8Á82 T 15 0Á01 32 0Á00 18Á77 0Á49 11Á26

may be increased in smaller areas due either to than 20 years may have low genetic variability, or genetic impoverishment, by the reduction of popula- heterozygosity, due to high inbreeding, resulting in tion sizes, or by other environmental changes that lower individual homeostasis (Wayne, Modi & increase as the habitat size decreases. O'Brien 1986; Clarke 1992; Hutchison & Cheverud According to Leary & Allendorf (1989), Evans 1995). Cheverud & Routman (1996), however, (1991) and Mùller (1993), the increase of FA in explain that epistasis for quantitative phenotypes morphological characters occurs in conditions of exhibiting dominance should be considered together genetic stress (high inbreeding, hybridization; Soule with heterozygosity in determining the genetic varia- 1967; Parsons 1992) and environmental stress (pollu- bility in a population. These authors found that tion, parasitism, low food availability; Valentine & epistasis in this case is added to the additive genetic Soule 1973; Ames, Felley & Smith 1979; Swaddle & variance and that it thus may increase the genetic Witter 1994), with evidence that the e€ects of both kinds of stress may be cumulative (Parsons 1992). variability. Larry, Routman & Cheverud (1997) Our study did not evaluate the genetic variability showed evidence for the heritability for FA levels # 2000 British of the populations studied, thus it was not possible among mice lineages and demonstrated the domi- Ecological Society to determine which type of stress most in¯uenced nance for quantitative trait loci associated with FA, Journal of Applied Ecology, 37, the relative FA levels in these fragments. Popula- thus high levels of FA may not necessarily re¯ect 1013±1028 tions that have been, in the main, isolated for more low genetic variability. 1020 Control forests 0á020 Fluctuating (a) Fragments asymmetry in 0á015 birds 0á010

0á005 2 10 × 0á000 IIIIII 0á020 (b)

Relative FA FA Relative 0á015

0á010

0á005

0á000 IIIIII

Fig. 2. Relative ¯uctuating asymmetry (mean and 1 SE) on wings (a) and tarsi (b) of birds from control forests and frag- ments. I, for all species; II, for species present in both forest types; III, for species present in both forest types with con-

trolled sample sizes. Values refer to the mean FAc (equation 1) among control areas and among fragments.

The relative FA levels in birds from fragmented strating the environmental basis of the stress forests may have been increased due to higher envir- a€ecting FA (Lens et al. 1999). onmental stress consequent upon forest clearance. There are large di€erences among species from Habitat change may increase pressures from preda- di€erent foraging guilds in their susceptibility to fragmentation e€ects in South American avian com- tors, competitors, parasites and disease (Rolstad munities. These di€erences are mainly in ecological 1991) and also may decrease food supplies, shelter characteristics, which are the key to understanding and nest site availability (Rappole & Morton 1985; and predicting which species will be under the great- Bierregaard & Lovejoy 1989; Tellerõ a & Santos est threat (Walters 1998). Most wildlife habitat mod- 1993). The level of forest degradation determined els that support conservation strategies emphasize FA alteration in seven bird species from other tropi- the importance of vegetation because selection of cal forest fragments that were evenly sized, demon- vegetative structure is believed to link bird popula-

Table 3. Comparisons of relative FA on wings and tarsi between control forests and fragments for the three analyses of communities. Community: I, all species included; II, only species present in both forest types; III, only species present in both forest types and controlled for species abundance. Values refer to the relative FA Â 102

Control  fragment Community Forest type (n) Trait Test P

I Control Wing t ˆ 4Á223 0Á004 (7) Tarsus t ˆ 2Á501 0Á031 Fragments Wing (5) Tarsus II Control Wing t ˆ 4Á263 0Á003 (7) Tarsus t ˆ 2Á641 0Á039 Fragments Wing (5) Tarsus # 2000 British III Control Wing t ˆ 5Á801 0Á001 Ecological Society (7) Tarsus t ˆ 2Á133 0Á031 Journal of Applied Fragments Wing Ecology, 37, (5) Tarsus 1013±1028 1021 0á020 Regression (a) M. AnciaÄes & 95% confidence M.AÃ. Marini 0á018 0á016

0á014

0á012

0á010

0á008 2 10

× 0á006 0á5 1á5 2á5 3á5 4á5 5á5

0á018 (b) Relative FA FA Relative 0á016

0á014

0á012

0á010

0á008

0á006

0á004 0á5 1á5 2á5 3á5 4á5 5á5 log area (ha)

Fig. 3. Relationship between relative FA on wings (a) and tarsi (b) for a bird community (FAc) and the forest size. FAc (equation 2) was estimated as the variance of the FA estimate described in equation 1.

tions with their environments. Changes in vegetation the foraging success of insectivorous species in parti- structure greatly a€ect foraging behaviour, espe- cular habitats (Robinson & Holmes 1984). Lens cially in insectivorous birds, which are usually extre- et al. (1999) observed that environmental degrada- mely specialized in their prey search and attack tion in¯uencing FA levels in birds was related to tactics (Cody 1985). As foliage distribution and changes in physiognomic and ¯oristic characteristics arthropod abundance vary with plant species, the in the fragments. These variables also in¯uenced ¯oristic composition of a site may strongly in¯uence selection of nesting sites and avoidance of predation

Table 4. The analysis of variance for foraging strata and diet comparisons among forest type, for relative FA on wings and tarsi. Only forest-dependent species present in both control forests and fragments were analysed. TU, terrestrial to under- storey; UM, understorey to medium strata; MC, medium strata to canopy; I, insectivorous; O, omnivorous. *P < 0Á05; **P < 0Á01

Foraging strata Diet Trait E€ect d.f. F Tukey's HSD d.f. F Tukey's HSD

Wing Forest type (1,774) 7Á48** ± (1,760) 4Á24* ± Foraging strata (2,774) 0Á26 ± ± ± ± Diet ± ± ± (2,760) 1Á50 ± Interaction (2,774) 0Á77 ± (2,760) 4Á77** I** # 2000 British Tarsus Forest type (1,743) 33Á90** ± (1,724) 26Á21** ± Ecological Society Foraging strata (2,743) 1Á37 ± ± ± ± Journal of Applied Diet ± ± ± (2,724) 1Á62 ± Ecology, 37, Interaction (2,743) 3Á64* TU** UM** (2,724) 1Á13* I** O* 1013±1028 1022 Table 5. The analysis of variance for the interaction between foraging strata and diet comparisons among forest type for Fluctuating relative FA on wing and tarsus. Only forest-dependent species present in both control forests and fragments were analysed. TU, terrestrial to understorey; UM, understorey to medium strata; MC, medium strata to canopy; I, insectivorous; O, asymmetry in omnivorous. *P < 0Á05; **P < 0Á01 birds Factor Foraging Strata UM TU Â UM UM Â MC

Diet I Â O I O

Trait E€ect d.f. F d.f. F d.f. F

Wing Forest type (1,412) 4Á45 * (1,337) 7Á77** (1,327) 0Á45 Foraging strata ± ± (1,337) 0Á03 (1,327) 0Á73 Diet (1,412) 1Á36 ± ± ± ± Interaction (1,412) 2Á37 (1,337) 0Á28 (1,327) 0Á809 Tarsus Forest type (1,400) 19Á59** (1,334) 16Á79** (1,306) 7Á67** Foraging strata ± ± (1,334) 5Á93* (1,306) 1Á02 Diet (1,400) 1Á25 ± ± ± ± Interaction (1,400) 0Á00 (1,334) 0Á03 (1,306) 0Á30

(Tellerõ a & Santos 1994). Decreased humidity abundance or activity of invertebrates in forests, observed in fragmented areas (Karr 1982; Tellerõ a & thus determining the abundance of insectivorous Santos 1993) led to changes in temperature and light birds. Insectivorous species richness tends to incidence in the forest interior, which a€ected spe- decrease where fragmentation has taken place in cies according to their nesting and foraging require- both the Atlantic and Amazonian Forests (Willis ments (Irwin 1994). Emlen et al. (1986) propose that 1979; Lovejoy et al. 1986; Stou€er & Bierregaard humidity and high temperatures determine the 1995). In the same regions, ground and understorey

Table 6. Species comparisons and correlations (Pearson correlation coecient) of relative FA on wings and tarsi. Compari- sons were conducted for FA among control forests (C) and fragments (F) and among characters within each forest type. Correlations were conducted among characters within each forest type. Means refers to relative FA  102

Control  fragment Wing  tarsus Species Forest type Trait Mean ‹ 1 se (n) t P t P r P

Dysithamnus mentalis C Wing 0Á86 ‹ 0Á17 (14) 0Á10 0Á33 1Á21 0Á24 0Á18 0Á54 Tarsus 0Á63 ‹ 0Á19 (16) 2Á19 0Á04 F Wing 1Á18 ‹ 0Á18 (14) 0Á2 0Á87 0Á31 0Á28 Tarsus 1Á20 ‹ 0Á21 (14) Conopophaga lineata C Wing 0Á52 ‹ 0Á11 (13) 2Á02 0Á03 0Á86 0Á40 0Á14 0Á66 Tarsus 0Á61 ‹ 0Á12 (14) 0Á47 0Á64 F Wing 0Á89 ‹ 0Á12 (35) 0Á95 0Á35 0Á06 0Á77 Tarsus 0Á79 ‹ 0Á14 (31) Platyrinchus mystaceus C Wing 0Á78 ‹ 0Á16 (31) 2Á15 0Á04 0Á88 0Á38 0Á02 0Á90 Tarsus 0Á80 ‹ 0Á13 (33) 2Á07 0Á05 F Wing 1Á26 ‹ 0Á20 (21) 0Á17 0Á86 0Á29 0Á22 Tarsus 1Á21 ‹ 0Á16 (20) Turdus albicollis C Wing 0Á80 ‹ 0Á12 (50) 1Á10 0Á28 1Á89 0Á06 0Á13 0Á38 Tarsus 0Á52 ‹ 0Á08 (51) 1Á86 0Á04 F Wing 0Á94 ‹ 0Á15 (34) 1Á51 0Á14 0Á21 0Á33 Tarsus 0Á69 ‹ 0Á10 (31) Tachyphonus coronatus C Wing 0Á67 ‹ 0Á12 (22) 0Á41 0Á68 0Á46 0Á65 0Á10 0Á68 Tarsus 0Á66 ‹ 0Á21 (21) 1Á24 0Á22 F Wing 0Á87 ‹ 0Á15 (40) 1Á03 0Á31 0Á03 0Á90 Tarsus 0Á85 ‹ 0Á13 (31) # 2000 British Trichothraupis melanops C Wing 0Á87 ‹ 0Á08 (85) 0Á66 0Á51 1Á83 0Á07 0Á08 0Á48 Ecological Society Tarsus 0Á64 ‹ 0Á06 (85) 2Á26 0Á03 Journal of Applied F Wing 0Á90 ‹ 0Á01 (34) 1Á48 0Á15 0Á24 0Á20 Ecology, 37, Tarsus 1Á17 ‹ 0Á24 (30) 1013±1028 1023 foraging birds are among those most a€ected by region Minas Gerais state, where it occurred in only M. AnciaÄes & habitat loss (Willis 1979; Bierregaard & Lovejoy 34% of the areas studied by Ribon (1998). These M.AÃ. Marini 1989). data are congruent with the greater relative FA The e€ects of forest fragmentation on relative FA observed in fragments, while alteration of FA only levels varied among species according to their fora- in the tarsus may re¯ect the stronger selection pres- ging guilds. This result also seems to be in accor- sure for symmetry on the wing than on the tarsus. dance with the pattern of their wing and tarsus use Dysithamnus mentalis forages in the medium strata in feeding and breeding behaviour. In general, insec- (Stotz et al. 1996) and may follow army ants (Willis tivorous species from the terrestrial and understorey 1984), which indicates that wings are relatively strata are the most sensitive to relative FA changes. important for the species' activities. However, stu- Thereafter, the greater the importance of a character dies on speci®c foraging tactics would provide more (wing or tarsus), the less it shows alteration on its reliable information in this respect. relative FA level. The absence of a correlation Conopophaga lineata is common in some frag- between wing and tarsus relative FA is in agreement ments in SaÄ o Paulo (Aleixo & Vielliard 1995) and with the results found by Evans, Martins & Haley Minas Gerais states (Ribon 1998), although Willis (1995) on hummingbirds Trochilus polytmus. It (1979) observed low abundance in previous studies shows that stress does not a€ect all structures simi- in the localities studied by Aleixo & Vielliard (1995). larly, nor do asymmetries in di€erent characters Changes in wing relative FA may re¯ect less selec- re¯ect the instability in di€erent developmental peri- tion pressure for symmetry on this characteristic ods (Palmer & Strobeck 1986). The relative FA in than in the tarsus, because it is a terrestrial species an individual character should not be taken as a that builds its nest and forages close to the ground measure of phenotypic quality for a bird because (Sick 1993). Competition for food seems to play an the genetic control occurs separately for di€erent important role in regulating the population characters, with individuals having, for example, dynamics in this species. Competition may, thus, be symmetric wings but asymmetric tarsi (Evans 1993; a source of environmental stress accounting for the Palmer 1994; Dufour & Weatherhead 1996). Evans, increased FA level observed in the fragments. Martins & Haley (1995) concluded that alteration in Individuals travel widely within their territories, wing asymmetry might be more representative of through horizontal, vertical and diagonal low disruption of developmental stability than asymme- perches, where they forage on small insects from the try in another character, for example the tarsus. litter. During the non-breeding season individuals However, selective pressure for symmetry is stronger feed solitarily, probably in order to increase prey on more important functional characters, which capture rates. However, litter does not o€er an vary considerably across species (Balmford, Jones & abundant food resource for this species, being better Thomas 1993). It should also be considered that exploited by arthropods that also forage on small increased FA in tarsus and wing might represent insects (Willis, Oniki & Silva 1983), and, in fragmen- fragmentation e€ects from di€erent origins, as tar- ted forests, competition between insectivorous birds sus development occurs only once in an individual's is expected to be greater as resource availability lifetime but feather moults occur every year. Tarsus decreases. FA could better estimate long-term genetic e€ects, The most abundant frugivorous species sampled in while wing FA could better indicate short-term this study (Chiroxiphia caudata, Manacus manacus environmental e€ects. However, the time scale ana- and Ilicura militaris) were commonly found in altered lysed in this study does not allow a di€erentiation forest patches (Aleixo & Vielliard 1995; Stotz et al. between these two processes. 1996; M. AnciaÄ es, unpublished data). This feature Platyrinchus mystaceus, Dysithamnus mentalis and demonstrates that these species probably have not Conopophaga lineata are insectivorous species that been a€ected by fragmentation, in agreement with showed alteration of relative FA levels. Platyrinchus the pattern shown by FA analyses. These species feed mystaceus was found in both forest types and it is on fruit plants commonly found on forest edges and usually observed in the lower parts of the under- other secondary growth areas, which represent an storey (Sick 1997). This species has disappeared abundant food resource for these birds (Foster 1987; from the 250-ha Santa Genebra fragment in SaÄ o M. AnciaÄ es, personal observation). Paulo state (Aleixo & Vielliard 1995), indicating The pattern found for Turdus albicollis and Tri- that it is sensitive to habitat reduction and isolation, chothraupis melanops may re¯ect their foraging supporting our ®ndings of increased relative wing habit. These species are omnivorous, eating fruit, and tarsus FA. insects and seeds from the understorey to the med- Dysithamnus mentalis was present in only two ium strata (Foster 1987; Sick 1993; Galetti & Stotz # 2000 British fragments in this study. Decreased population sizes 1996). They seem to be less sensitive to fragmenta- Ecological Society and local extinctions have been observed in isolated tion, probably because as more generalist species Journal of Applied Ecology, 37, forests (Aleixo & Vielliard 1995), and fragment size they rely on a greater variety of food sources, and, 1013±1028 appears to limit the species' distribution at VicË osa in fact, they have persisted in fragmented areas 1024 (Willis 1979; Laurance 1991). Tachyphonus corona- species most suited for the application of FA as con- Fluctuating tus showed no di€erences in relative FA levels servation indices, as well as in verifying the genetic asymmetry in among forest types, which may be an e€ect of its and environmental contribution to the origin of birds foraging strata. It is also omnivorous (Sick 1993; increased FA. Galetti & Stotz 1996) but forages from the medium strata to the canopy, and species occupying these strata are among those less a€ected in fragmented Acknowledgements habitats (Willis 1979; Bierregaard & Lovejoy 1989; This study was supported by USWF, PRPq-UFMG Laurance 1991). and CNPq grants. M. AnciaÄ es received a graduate The ability to disperse has been considered the fellowship from CAPES and FAPEMIG, and M.Aà . principal characteristic determining the sensitivity of Marini received a research fellowship from CNPq. a species to fragmentation (Walters 1998). There are We are grateful to the following ®eld stations and few data available regarding movement patterns of their sta€ for permission and assistance with our insectivorous species. Dysithamnus mentalis and Pla- study: Instituto Ambiental do Parana , Companhia tyrinchus mystaceus have been recorded moving a Paranaense de Eletricidade, Companhia de Sanea- maximum of 700 and 300 m, respectively, in frag- mento de Minas Gerais, FundacË aÄ o `O Botica rio' de mented landscapes from Minas Gerais state, ProtecË aÄ o aÁ Natureza, Parque Nacional do Itatiaia, whereas the frugivore Antilophia galeata is known to Universidade Federal de VicË osa, FundacË aÄ o J.P. de have crossed about 700 m in the same region as Pla- Oliveira and Instituto Florestal de SaÄ o Paulo. We tyrinchus mystaceus (Andrade 1999; M. Aà . Marini, are equally grateful to the landowners of the unpublished data). It is not known whether insecti- Fazenda Retiro and Fazenda Vale de BencË aÄ os. We vore species are more a€ected by isolation distances thank several people involved in the ®eld work, spe- than other groups. cially P. Cordeiro, V. Tavares, F. Straube, A. Our results, nevertheless, show that species have Urben-Filho, G. Reis, F. Teixeira, D. Kijawara, D. been in¯uenced by fragmentation more strongly Couto, M. Del Sarto, C. Meirelles, J. Ferreira, A. than has been previously documented in the litera- Salim, R. Ribon, R. Ribeiro, C. Duca, T. Aguilar ture (Terborgh 1974; Willis 1979; Bierregaard & and A. Bom®m. R. AssuncË aÄ o, M. Balassiano, A. Lovejoy 1989). Karr (1982) noticed that even rela- Paglia and G. Marroig made important suggestions tively abundant species of undergrowth forests are and helped with the statistics. F. Silveira, F. Fernan- lost as a result of fragmentation, in contrast to the dez, R. Cavalcanti, P. Cordeiro and F. Straube general correlation between rarity and extinction kindly revised previous drafts of the manuscript. We probability (Terborgh & Winter 1980). The relative are very thankful to D. Yanega and O. Komar for FA levels shown by those species indicates that improving the English version, and to G. Kerby, S. there has been a disruption in developmental stabi- Ormerod, R. Prum and two anonymous referees for lity even in species commonly found in fragmented substantial comments and editing of the text. forests. Consequently, FA may be used to detect species that are being a€ected by fragmentation but have not been identi®ed by studies relying on References indexes such as the relative abundance. Indeed, Clark (1995) suggested that FA could be used as an Aleixo, A. & Vielliard, J.M.E. (1995) ComposicË aÄ o e dinaà - early warning system, because it may detect pro- mica da avifauna da Mata de Santa Genebra, Campi- nas, SaÄ o Paulo, Brasil. 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# 2000 British Ecological Society Journal of Applied Ecology, 37, 1013±1028 1027 Appendix 1 M. AnciaÄes & Relationship between species sampled in each locality and their characteristics. HD, habitat dependence; FS, M.AÃ. Marini foraging strata; DT, diet type. See Table 1 and text for locality and characteristic codes. Scienti®c authorities followed Hellmayr (1924±1938). *Species analysed for measurement error estimates.

Taxa HD FS DT Localities

FAMILY DENDROCOLAPTIDAE Dendrocincla turdina (Lichtenstein 1818) * 3 U/M I C1,C2,C5,C7 Sittasomus griseicapillus (Temminck 1821) 3 M I C1,C2,C3,C6,C7,F2 Xiphocolaptes albicollis (Vieillot 1818) 3 M I C3 Dendrocolaptes platyrostris (Spix 1824) 3 M I C1,C3,C5,C6 Campilorhamphus falcularius (Vieillot 1822) 3 U/M I F1 Lepidocolaptes fuscus (Vieillot 1818)* 3 U/M I C1,C2,C3,C4,C5,C6,C7,F2,F4 FAMILY FURNARIIDAE Synallaxis spixi (Sclater 1856) 3 U I C3 Synallaxis ru®capilla (Vieillot 1819) 3 U I C4,F4 Phacellodomus erytrophthalmus (Wied 1821) 2 U/M I F1 Anabazenops fuscus (Vieillot 1816) - M I C6 Philydor atricapillus (Wied 1821)* 3 M I C2,C4,C5,C6,C7 Philydor lichtensteini (Cabanis & Heine 1859) 3 M I C1 Philydor rufus (Vieillot 1818) 3 M I C3,C5 Automolus leucophthalmus (Wied 1821)* 3 U I C1,C2,C5,C6,C7,F2,F4,F5 Xenops minutus (Sparrman 1788) 3 U/M I C4,C7 Xenops rutilans (Lichtenstein 1823) 3 U/M I F1,F4,F5 Sclerurus scansor (Me ne trieÁ s 1835) 3 T I C1,C2,C3,C4 Lochmias nematura (Lichtenstein 1823) 3 T I C3 FAMILY FORMICARIIDAE Mackenziana severa (Lichtenstein 1823) 3 U I C1 Thamnophilus doliatus (Hellmayr 1903) 2 U/C I F5 Thamnophilus punctatus ( Hellmayr 1885) 3 U/M I F4 Thamnophilus caerulescens (Pelzeln 1868) 3 U/M I C1,C3,F2,F3,F4 Dysithamnus mentalis (Temminck 1823)* 3 U/M I C1,C4,C6,C7,F2,F4 Myrmotherula gularis (Spix 1825) 3 U I C5,C6,C7 Myrmotherula unicolor (Me ne trieÁ s 1835) 3 M I C2,C4,C5,C7 Drymophila ochropyga (Hellmayr 1906) 3 U I C3 Drymophila squamata (Boucard & Berlepsch 11892) 3 U I C2,C4,C7 Pyriglena leucoptera (Vieillot 1818)* 3 U I C1,C2,C3,C4,F2 Myrmeciza loricata (Lichtenstein 1823) 3 T I C2,C3,C6 Myrmeciza squamosa (Pelzeln 1868) 3 T I C4,C7 Formicarius colma (Boddaert 1783) 3 T I C4 FAMILY CONOPOPHAGIDAE Conopophaga lineata (Wied 1831)* 3 U I C1,C3,C4,C6,F1,F2,F3,F4 Conopophaga melanops (Vieillot 1818) 3 U I C2,C5,C6,C7 FAMILY TYRANNIDAE Phyllomyias virescens (Allen 1889) 3 C I F5 Camptostoma obsoletum (Temminck 1824) 1 C I F5 Myiopagis caniceps (Swainson 1837) 1 U I F5 Elaenia spectabilis (Pelzeln 1868) 3 U O F5 Mionectes ru®ventris (Cabanis 1846) 3 U/M O C2,C3,C4,C6,C7,F1,F2, Leptopogon amaurocephalus (Tschudi 1846) 3 U/M I C2,C4,C6,C7,F1,F2,F5 Corythopis delalandi (Lesson 1830) 3 T I C1,F1,F2,F4,F5 Hemitriccus diops (Temminck 1822) 3 M I C3 Hemitriccus orbitatus (Wied 1831) 3 T/C I C1,C2,F4 Tolmomyias sulphurescens (Spix 1825) ± ± I C1,C3,C6 Platyrinchus mystaceus* (Vieillot 1818) 3 M/C I C1,C2,C3,C4,C5,C6,C7,F1,F2,F4 Myiobius barbatus (Wied 1821) 3 C I C4,C6,C7 Myiobius atricaudus (Lawrence 1863) 3 U/M I C3 Myiophobus fasciatus (Ihering 1907) 3 U I F1,F5 Lathrotriccus euleri (Cabanis 1868) 3 U/M I C3,F2,F4 Cnemotriccus fuscatus (Wied 1831) 3 U/M I F5 Knipolegus cyanirostris (Vieillot 1818) 3 M I C3 Satrapa icterophrys (Vieillot 1818) 3 C I F5 Rhytipterna simplex (Lichtenstein 1823) 3 M/C I C7

# 2000 British Ecological Society Journal of Applied Ecology, 37, 1013±1028 1028 Appendix 1 (cont'd ) Fluctuating asymmetry in Taxa HD FS DT Localities birds FAMILY PIPRIDAE Pipra fasciicauda (Hellmayr 1915) 3 U/M F F5 Antilophia galeata (Lichtenstein 1834) 3 M/C F F2 Chiroxiphia caudata (Shaw & Nodder 1793)* 3 U/M F C1,C2,C3,C4,C5,C6,C7,F1,F2, F3,F4 Ilicura militaris (Shaw & Nodder 1808)* 3 M/C F C2,C3,C4,C5,F2 Manacus manacus (Desmarest 1806) 3 U F C2,C4,F1,F3 Schi€ornis virescens (Lafresnaye 1838) 3 U I C1,C2,C3,C4,C6 FAMILY COTINGIDAE Laniisoma elegans (Thunberg 1823) 3 M/C O C7,F2 FAMILY TROGLODYTIDAE Thryothorus longirostris (Vieillot 1819) 3 U I F1 Troglodytes aedon (Vieillot 1807) 1 T/U O F1 FAMILY MUSCICAPIDAE Subfamily Turdinae Platicychla ¯avipes (Vieillot 1818)* 3 M/C O C6,C7 Turdus ru®ventris (Vieillot 1818) 1 T/C O C1,C4,F1,F2,F3,F4 Turdus leucomelas (Vieillot 1818) 2 T/C O F1,F2,F5 Turdus amaurochalinus (Cabanis 1851) 2 T/C O C1,F3,F5 Turdus albicollis (Vieillot 1818)* 3 U/M O C1,C2,C3,C4,C5,C6,C7,F1,F3, F5 FAMILY EMBERIZIDAE Subfamily Parulinae Geothlypis aequinoctialis (Vieillot 1807) 1 U I F5 Basileuterus ¯aveolus (Baird 1865) 3 T/U I C1,F2,F3 Basileuterus culicivorus (Swainson 1837)* 3 U/M I C1,C2,C3,C4,C5,C6,C7,F1,F5 Basileuterus hypoleucus (Swainson 1837) 3 U/M I F2,F3,F4 Phaeothlyps rivularis (Wied 1821) 3 T I C4,C5 Subfamily Coerebinae Coereba ¯aveola (Cabanis 1851) 1 C O C4,F3 Subfamily Thraupinae Pyrrhocoma ru®ceps (Strickland 1844) 3 U I F5 Thlypopsis sordida (Lafresnaye & d'Orbigny 1837) 2 U/C O F1,F3 Hemithraupis guira (Linnaeus 1766) 3 C O F5 Tachyphonus cristatus (Spix 1825) 3 C O C2,C7 Tachyphonus coronatus (Vieillot 1822)* 3 M/C O C1,C3,C4,C5,C6,C7,F1,F3,F4,F5 Trichothraupis melanops (Vieillot 1818)* 3 U/M O C1,C2,C3,C4,C5,C6,C7,F2,F3,F4,F5 Habia rubica (Vieillot 1817)* 3 U/M O C1,C2,C4,C5,C6,C7,F3 Ramphocelus bresilius (Linnaeus 1766) 2 U/M O C4,F1 Thraupis sayaca (Linnaeus 1766) 2 C O F1 Thraupis cyanoptera (Vieillot 1817) 3 C O C4 Stephanophorus diadematus (Temminck 1819) 3 U/C O C5 Pipraeidea melanonota (Vieillot 1819) 3 M/C O F5 Euphonia violacea (Linnaeus 1758) 3 C F C4 Euphonia pectoralis (Latham 1801) 3 C F C4,C5,C6 Tangara seledon (MuÈ ller 1776)* 3 C O C4 Tangara cyanocephala (MuÈ ller 1776) 3 C O C4 Tangara desmaresti (Vieillot 1819) 3 C O C3 Tangara cyanoventris (Vieillot 1819) 3 C O C6,F1 Tangara cayana (Linnaeus 1766) 1 U/C O F1 Conirostrum speciosum (Temminck 1824) ± C O F5 Subfamily Emberizinae Haplospiza unicolor (Cabanis 1851)* 3 M/C G C1,C3,C4,C5,C6,F3 Amaurospiza moesta (Hartlaub 1853) 3 T/U G C1,C4 Sporophila caerulescens (Vieillot 1817) 1 U O F3 Arremon semitorquatus (Swainson 1837) 3 T I C5 Arremon ¯avirostris (Swainson 1837) 3 T I C1 Saltator similis (Lafresnaye & d'Orbigny 1837) 2 M/C G C1,C2,C3,C4,C6,F1,F3,F4,F5 FAMILY VIREONIDAE Cyclarhis gujanensis (Tschudi 1845) 2 M/C O F2 Hylophilus poecilotis (Temminck 1822) 3 M/C O C3

# 2000 British Ecological Society Journal of Applied Ecology, 37, 1013±1028