ORIGINAL ARTICLE

Edge effect and structure of mixed-species bird flocksin an Afrotropical lowland forest

Guillaume Peron Æ Pierre-Andre Crochet

Received: 21 October 2008 / Revised: 20 November 2008 / Accepted: 12 January 2009 / Published online: 10 February 2009

� Dt. Ornithologen-Gesellschaft e.V. 2009

Abstract Avian mixed-species flocks are a dominant

feature of tropical moist forests, yet their cost–benefit

balance and habitat dependence in Africa are not fully

documented. We recorded the composition of mixed-spe-

cies bird flocks in a pristine Afrotropical lowland forest site

in Salonga NP, DRC. Our data showed that at least four

types of flock existed, one of which specialized on edge

habitats. We used multivariate analyses to further charac-

terize edge effect on the most documented mixed-species

flock type and found a significant effect on flock compo-

sition. While neither species guild nor preferential foraging

stratum played an important role in flock participation, the

nucleus role was played by a different species at the edge

and in the interior, and both species abundance and asso-

ciations were habitat-dependant, suggesting ‘‘domino

effects’’ on the structure of mixed-species flocks.

Keywords Flock size � Heterospecific � Multi-species �Mutualism � Salonga

Introduction

Mixed-species flocks are social groups of individuals of

several different species that travel together through their

habitat. They occur in many vertebrate taxa from fishes

(Lukoschek and McCormick 2002) to mammals (Stensland

et al. 2003; Bearzi 2006) and range from temporary

associations (Nemeth and Moore 2007) to long-term rela-

tionships with multi-species territoriality (Morse 1970;

Jullien and Thiollay 1998). In birds, mixed-species flocks

are found in a wide variety of forested ecosystems, but they

reach their maximum development in communities of

tropical moist forests, of which they are a dominant feature

(Powell 1989).

Mixed-species flocking has been puzzling ornithologists

for decades, and the fitness advantages of mixed-species

flocking behaviour are still only partially understood.

Jullien and Clobert (2000) obtained results suggesting an

enhanced survival in obligate flocking species, and while

some studies showed that individuals fed at higher rates

inside than outside mixed-species flocks (Herrera 1979;

Hino 1998; Thomson and Ferguson 2007), others suggested

that the benefit is the reduction in predation risk (e.g.

Thiollay 1999). The most widely considered hypotheses are

advantages of flock size when the number of individuals per

species is limited (predation risk reduction: Hamilton 1971;

Lazarus 1979; foraging enhancement: Clark and Mangel

1984) and mutualistic interactions between species (for

foraging enhancement: Waite and Grubb 1988; Brown and

Brown 1996; Hino 1998; Bearzi 2006; but also to some

extent for predation risk reduction: Munn 1986). These

hypotheses lead to different predictions about associations

of particular species in flocks (Hutto 1994).

Flock composition is also likely to be determined by

environmental factors, through species requirements

(‘‘species co-dependency on environmental variables’’:

Hutto 1994). In tropical Asia, flocks exhibit a variation in

composition along a disturbance gradient (Lee et al. 2005),

while in South America, forest fragmentation leads to a

change in composition via both modifications of the local

Communicated by J. Fjieldsa.

G. Peron (&) � P.-A. Crochet

Equipe Biometrie et Biologie des Populations,

Centre d’Ecologie Fonctionnelle et Evolutive,

CNRS UMR 5175, 1919 Route de Mende,

34293 Montpellier, France

e-mail: peron_guillaume@yahoo.fr;

guillaume.peron@cefe.cnrs.fr

123

J Ornithol (2009) 150:585–599

DOI 10.1007/s10336-009-0376-4

avifauna and of the flocking propensity (Stouffer and

Bierregaard 1995; Stratford and Stouffer 1999). In an

Afrotropical forest site, Dale et al. (2000) found an effect

of distance to edge on the understorey bird community,

which would probably have been reflected in flock com-

position. There are few other studies about the edge effect

on the Afrotropical avifauna, especially focusing on mixed-

species flocks of insectivorous birds. Yet, as suggested

above, there are reasons to believe that the on-going

deforestation (Achard et al. 2002) and associated habitat

changes will impact on flock structure as it does in other

tropical ecosystems (Stouffer and Bierregaard 1995;

Maldonado-Coelho and Marini 2004), potentially acceler-

ating the impoverishment of avian communities, if flocking

is important for the maintenance of any given species

(Powell 1989). Furthermore, the role of ‘‘nucleus’’ species

(species that maintain cohesion, attract other flock mem-

bers and lead the flock; Moynihan 1962) has been little

studied for what concerns the changes between habitats:

are the nucleus species the same at the edge and in the

interior and what happens if the nucleus species becomes

scarce (Hart and Freed 2003)? More generally, are the

associations between different species habitat-dependant?

Here, we used data on flock composition from a seldom

studied region, the Afrotropical lowland forest of the

Congo basin, in a pristine habitat with little human

encroachment, to study the variation in flock structure

between edge and interior habitats. The first aim was to

detect and characterise the edge effect on flock structure,

through species abundance and/or species associations,

potentially highlighting a change in nucleus species.

Second, in an Afrotropical context, little is known about

potential proximal and ultimate mechanisms leading to

associations of particular species. If birds flock to gain

access to the greatest possible flock size (Clark and Mangel

1984), there should be much reduced influence of flock

composition on flock participation (Pomara et al. 2007),

whereas if species compatibilities and complementarities

drive mixed-species flocking, flock composition should

reflect species-specific mutualistic interactions (Hutto

1994), and we would expect in particular different guilds to

associate (Brosset and Erard 1986; Munn 1986), so that

they can benefit from their different skills (Giraldeau 1984;

see also Waite and Grubb 1988). We thus studied potential

determinants of flock participation: effect of the guild

(main insectivore feeding technique; King and Rappole

2001), of the preferential feeding strata (height at which the

species takes most of its prey; Jullien and Thiollay 1998),

of the intrinsic preference for edge or interior (habitat

preference; King and Rappole 2000) and of the flock spe-

cies richness (number of species in the flock; Maurer

1984). All these effects also constitute potential ways

through which habitat can impact on flock structure.

Methods

Study site

A description of the site of Lui Kotal (02�45.6100S,

0�22.7230E) appears in Hohmann and Fruth (2003) and

Fruth et al. (2003). This site is situated in the Salonga

National Park, in the Bandundu province of the Democratic

Republic of the Congo. It is a lowland rainforest with a low

canopy (main tree species: Staudtia stipitata, Greenwayo-

dendron suaveolens, Scorodophloeus zenkeri, Anonidium

manni and Parinari glabra; homogeneous stands of

Monopetalanthus pteridophyllus occur on poor sandy soils

and of Gilbertiodendron sp. and Brachystegia sp. on terra

firma soils). The understorey is generally dense (dominant

family: Rubiaceae; extensive areas are also covered with the

liana Haumania sp.). The rainforest there is dotted with

more or less large areas of savannah maintained open by

regular fires, and with areas of open marshes; it is also

crossed by rivers. There are thus naturally-occurring large

tracts of edge forest. We had access to both edge (considered

to be the 50-m-wide fringe around a man-made clearing and

the adjacent bank of a medium-sized river), and interior

(accessed through a network of forest trails of[50 km). The

sampled area was larger in the interior than in the edge

situation (magnitude of the areas within reach of the

observer: about 100 ha in the interior and 1 ha at the edge).

Although the limited area of edge habitat makes it difficult

to assert that flocks sampled there were completely inde-

pendent, we are confident about the fact that several flocks

shared this area as part of their home-range (Poulsen 1996a;

see also Brosset and Erard 1986 for a discussion about

shared home-range in ant-following flocks in Gabon). As a

confirmation of this assumption, variance in flock com-

position was not lower at the edge than in the interior (see

‘‘Results’’), contrary to what would have been predicted if

the number of independent flocks was much different.

Study species

The species commonly encountered in flocks (Table 1) are

territorial, at least during reproduction, and some, such as

Icterine Greenbul Phyllastrephus icterinus, show long-

lasting territory- and mate-fidelity (Brosset and Erard

1986). Flock participation is then likely determined by

territory boundaries (Jullien and Thiollay 1998; Pomara

et al. 2007; but see Poulsen 1996a). Most species from the

Afrotropical lowland forest are known to breed all year

round, with a peak of laying linked to the main rain season

(Brosset and Erard 1986). The main dry season is consi-

dered to be a period of low reproductive activity for forest

species; territorial behaviours such as singing decrease in

intensity during this season (Brosset and Erard 1986). We

586 J Ornithol (2009) 150:585–599

123

(G.P.) recorded data during June and July 2006, which

constitute the beginning of the main dry season. There was

thus little reproductive activity during data recording, and

hence little interference of this activity with flock partici-

pation (Develey and Peres 2000).

Information on species characteristics and requirements

(‘‘Appendix 1’’) were obtained from handbooks (Fry et al.

1988; Keith et al. 1992; Urban et al. 1997; Fry and Keith

2000, 2004). Using this information, we classified species

a priori following three criteria: (1) preference for edge or

interior, (2) preference for canopy (crown of tallest tree, or

above 20 m), mid-strata, or ground (below 3 m), and (3)

main insectivore feeding technique or ‘‘guild’’ (leaf-

gleaning, searching, sallying or bark-gleaning; nectari-

vores–insectivores and frugivores–insectivores were

classified according to their technique when catching

insects). The four guilds are derived from Thiollay (1999)

and Dale et al. (2000), where they are further described.

Data collection

A mixed-species flock is defined as at least two different

species foraging and moving in a similar direction, with

flock members less than 10 m apart (Morse 1970). This

definition is relatively large and includes temporary asso-

ciations. Each time such a group of individuals was

opportunistically detected from the network of trails, it was

followed for as long as possible. The species composing it

were recorded, except when the conditions (distance to

the observer, duration of the observation, vegetation)

obviously prevented the exhaustive determination of

all member species. The environmental variable (edge/

interior) was also recorded. On one occasion, the flock

moved from the interior to the edge; in this instance, it was

followed for a longer time period at the edge and was hence

recorded as an edge flock.

Only species contacted for more than 10 min were

recorded, which represents a trade-off between the risk of

including an individual not actually associating with the

flock and the difficulty of following the flock for a long

period in the vegetation. This 10-min contact period means

that temporary associations that last only for the time that a

flock spends in the attendants’ territory were included. We

only excluded some observations of obviously non-flock-

ing individuals that occurred by chance in the vicinity of a

flock that crossed their territory (e.g. Stiphornis erythro-

thorax, Illadopsis rufipennis).

Despite the difficulty of assessing accurately the number

of birds present in dense vegetation, we believe that at least

the different species could be detected (the very similar

Xavier’s and Icterine Greenbuls Phyllastrephus xavieri/ic-

terinus were pooled together, and the rope squirrels

Funisciurus sp. were not recorded). This means that we

collected no precise information on the actual size of the

flock (number of individual birds), but we did record the

flocks’ species richness (number of member species). We

did not record more than one flock per day, except when the

distance was at least 3,000 m between two flock encounters.

Statistical analysis

The analysis of flock composition was performed using

tools developed for community ecology. Statistical tests

were performed with R (R Development Core Team 2005).

Table 1 Core sets of species

These are species found in more

than 20% of the flocks sampled

in one or two of the habitats.

When the 20%-threshold was

exceeded in one habitat only,

we speak of species important at

the edge/in the interior only

Edge and Interior correspond to

the frequency in the flocks

sampled in the corresponding

situations

Species important in both edge and interior Edge Interior

Dicrurus atripennis Shining Drongo 0.30 0.24

Phyllastrephus icterinus Icterine Greenbul 0.33 0.74

Criniger calurus Red-tailed Bulbul 0.30 0.21

Deleornis axillaris Grey-headed Sunbird 0.63 0.37

Species important in interior only

Campethera nivosa Buff-spotted Woodpecker 0.11 0.26

Bleda syndactyla Common Bristlebill 0.0 0.21

Bleda n. notatus Green-tailed Bristlebill 0.0 0.21

Terpsiphone rufiventer Black-headed Paradise-Flycatcher 0.19 0.29

Species important at the edge only

Tockus camurus Red-billed Dwarf Hornbill 0.33 0.11

Coracina azurea Blue Cuckoo-Shrike 0.37 0.03

Terpsiphone batesi Bates’s Paradise-Flycatcher 0.26 0.13

Andropadus gracilirostris Slender-billed Greenbul 0.26 0.11

Hedydipna collaris Collared Sunbird 0.30 0.03

J Ornithol (2009) 150:585–599 587

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Statistical tools for multivariate analyses were obtained

from the R-package VEGAN (Oksanen et al. 2007). We

conducted the analysis in three phases: (1) core species and

flock species richness, (2) multivariate analysis, and (3)

pair-based analysis of interspecific associations.

Core species and flock species richness

‘‘Core’’ or ‘‘important’’ species were defined as species

attending 20% or more of the observed flocks (which only

partially matches the definition for ‘‘nucleus’’ species;

Moynihan 1962). For the purpose of this study, we exam-

ined core species separately in the edge and the interior

situations. Flock species richness is the total number of

species in a flock.

Multivariate analyses

For these analyses, each flock was treated as an ‘‘individual’’

and all species recorded at least twice as ‘‘variables’’. As

outliers are known to distort the result of multivariate anal-

yses (Tabachnik and Fidell 1989), and because they

potentially have interesting ecological properties, we first

performed an outlier analysis (detection of flocks whose

dissimilarity with the rest of the dataset exceeded a cut-off

value). We used Sorensen distance (or Bray–Curtis distance;

McCune and Grace 2002) as a measure of dissimilarity with

cut-off value as two standard deviations from the mean. It

revealed four outlier flocks, which had marked ecological

characteristics (see ‘‘Results’’). To reduce in our sample the

variance linked with such ecological differences between

flocks, we chose to discriminate all flocks that were allied to

the strong outliers by lowering the cut-off value to 1.2 9 SD.

The following analyses were performed on the remaining 50

flocks, hereafter ‘‘typical understorey flocks’’.

We used non-metric multidimensional scaling (NMDS)

to ordinate sample units (remaining flocks, n = 50) in

species space (40 species) based on presence–absence of

species in flocks (McCune and Grace 2002). NMDS is a

computation-intensive optimisation method that minimises

the departure from monotonicity in the relationship between

the original dissimilarity in the n samples and their position

on a reduced k-dimensional ordination space. It is similar in

general purpose and philosophy to principal component

analysis (i.e. creating variables summarising the dissimi-

larities in species composition of the flocks), but reduces the

dimension of the data in a nonlinear fashion, and allows the

use of non-parametric tests. We used Sorensen distance as

dissimilarity measure (McCune and Grace 2002). To decide

the final dimension of the ordination space (k), we measured

the stress of the ordination procedure for k running from 1 to

6. The minimal stress was obtained for k equalling 4; there

were thus 4 axes in the final ordination space.

Multi-response permutation procedure (MRPP; Mielke

and Berry 2001) was then used to provide a non-para-

metric multivariate test of differences in the mixed-

species flocks among habitats. MRPP is based on an

analysis of a rank-transformed distance matrix, with the

same distance measure as NMDS (McCune and Grace

2002), and focuses on testing if the within-habitat aver-

age dissimilarities are smaller than predicted at random.

The observed mean distance among flocks of different

habitats is compared to the distribution of the distances

among habitats obtained from datasets where flocks are

assigned to each habitat category at random. This tech-

nique has already been used for the analysis of mixed-

species flock composition by, e.g., Lee et al. (2005). A

significant MRPP test would indicate that flock compo-

sition is markedly more similar within than between

habitats.

In the case of the effect of species richness of the flocks,

the explanatory variable was continuous, requiring the use

of a non-parametric multivariate analysis of variance

(MANOVA) that allows the user to fit linear models to

distance matrices (Anderson 2001; function adonis in

VEGAN). A significant test of the MANOVA would

indicate that composition of the flocks varies along the

gradient of species richness, i.e. that some species are more

often associated with poor or diverse flocks than expected

at random.

MRPP was also used on species ordination (i.e. on the

transposed observation matrix) to test for the influence of

species’ guilds on flock participation. A significant MRPP

P value for feeding techniques would indicate that flocks

attended by species of the same guild are more similar

than expected at random, i.e. that species associate pref-

erentially inside their guild. To formally test the

hypothesis that species associate with members of dif-

ferent guilds, we studied nearest neighbours in the species

ordinated space. Nearest neighbours of a given species

had to be present in at least two samples to be consi-

dered. We then performed a Fisher’s exact test on the

table ‘‘guild of the species/guild of its nearest neighbour’’

containing in cell (i, j) the number of neighbour pairs

with one species from guild i and one species from guild

j. This test indicated whether some pairs of guilds were

more or less often found together than expected at ran-

dom, given the distribution of the guilds among the study

species. If the MRPP was non-significant and the Fisher’s

test was significant, species associated preferentially with

at least one member of a different guild. The alternative

hypothesis was that species associated independently of

their guild and corresponded to non-significance of both

tests. The effect of other species characteristics (prefer-

ential strata, preference for edge) was tested in the same

way.

588 J Ornithol (2009) 150:585–599

123

Pair-based analysis of interspecific associations

Analyses that highlight the associations between individ-

ual pairs of species permit more detailed insight into the

potential behavioural mechanisms underlying flock com-

position than larger-scale multivariate analysis, and we

used them to highlight the changes in species association

between edge and interior. In particular, as nucleuses

attract other species, they should be found associated with

a comparatively great number of species (Moynihan

1962).

Study of pair-based associations was performed fol-

lowing the methodology described and used in, e.g.,

Hutto (1994) and Hart and Freed (2003), based on a

coefficient of interspecific association and a Fisher’s

exact test. We performed the analyses separately for

edge and interior, so that we could observe the change in

species association between these two habitats. More-

over, from the multivariate analyses, we learnt (see

‘‘Results’’) that habitat was a confounding environmental

factor (species co-dependency on environmental vari-

ables: Hutto 1994; King and Rappole 2000) which would

have biassed the analysis.

In order to detect whether species attracted or excluded

each other, we computed a coefficient of interspecific

association for each pair of species (Cole 1949). But we

modified Cole’s coefficient in order to have C(A,B) =

C(B,A):

C A;Bð Þ ¼ a� d � b� cffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi

aþ bð Þ aþ cð Þ d þ cð Þ d þ bð Þp ;

where a represents number of flocks where both species are

found, b the number of flocks in which only species A is

found, c the number of flock in which only B is found and d

the number of flocks in which neither is found. The coef-

ficient varies between -1 for completely exclusive species

and ?1 for obligate associated species. Its value is 0 for

species that associate randomly given their frequency in

flocks.

We further evaluated the significance of each associ-

ation using Fisher’s exact tests. This test was influenced

by sample size, which prevented the detection of

associations between rare and frequent species due to

the lack of statistical power. On the contrary, associa-

tions of species with similar frequencies were correctly

retrieved.

A positive association is hereafter a pair of species for

which the Cole’s coefficient is positive and the Fisher’s

test significant. A negative association is a pair of

species for which the Cole’s coefficient is negative and

the Fisher’s test significant. A species concentrating

positive associations was considered a candidate nucleus

species.

Results

Species richness of the flocks and core sets of species

As can be seen from ‘‘Appendix 1’’, only a handful of

species were regular members of mixed-species flocks.

Seventy-six species were seen in at least one mixed-species

flock, but only 47 occurred twice or more. The overall

mean specific diversity of the flocks was 5.6 species and

the most diverse flock had 13 species (Fig. 1). Table 1

shows the 13 species that were present in more than 20% of

the flocks (edge or interior). These species are hereafter

referred to as ‘‘core’’. Four species were in the core group

both at the edge and in the interior [Icterine Greenbul,

Grey-headed Sunbird Deleornis axiliaris, Shining Drongo

Dicrurus atripennis and Red-tailed Greenbul (RTGR)

Criniger calurus]. Two core species were found only in the

interior [Common Bristlebill (COBR) Bleda syndactila and

Green-tailed Bleda n. notatus]; no core species was strictly

restricted to edge habitats.

Among the rare flock attendants (those present in less

than 20% of the flocks), 21 species showed a higher fre-

quency at the edge than in the interior, 5 of them being

present only at the edge (‘‘Appendix 1’’). Only 11 species

were more frequent in the interior, of which 7 were only

found in the interior. As a result, species richness was

greater in the edge situation (Fig. 1; Table 2; Welch two-

sample t test: t54 = 2.6, P = 0.01).

Different flocking systems

Among the 65 flocks recorded, the outlier analysis revealed

four ‘‘strong’’ outliers (deviation from the mean [2SD).

These outlier flocks corresponded to clear ecological

groups: two were flocks of canopy feeders that aggregated

on emerging flying termites (Brosset and Erard 1986; Korb

0

2

4

6

8

10

12

14

16

2 3 4 5 6 7 8 9 10 11 12 13

Species richness

Fig. 1 Species richness of the 65 flocks recorded. Shaded areasflocks sampled in the interior. Unfilled areas flocks sampled at the

edge

J Ornithol (2009) 150:585–599 589

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and Salewski 2000) and two were constituted of ground

feeders that followed ant-swarms to catch the invertebrates

they flush (Brosset and Erard 1986; Dobbs and Martin

1998). Flocks of canopy feeders included species such as

African Forest-Flycatcher Fraseria ocreata, Cassin’s Mal-

imbe Malimbus cassini, Yellow-mantled Weaver Ploceus

tricolor and Blue-throated Roller Eurystomus gularis.

Ground feeders flocks had species such as Brown Illodopsis

Illadopsis fulvescens, Fire-crested Alethe Alethe castanea,

Rufous Flycatcher-Thrush Stizorhina fraseri, Red-tailed

Ant-Thrush Neocossyphus rufus, Common Bristlebill and

Green-tailed Bristlebill. Lowering the cut-off value of the

outlier analysis also discriminated some flocks containing

only species of open areas and forest edge such as Collared

Sunbird Hedydipna collaris, Olive-bellied Sunbird Cynniris

chloropygius, Yellowbill Ceuthmochares aereus, Rufous-

bellied Helmetshrike Prionops rufiventris, and Sooty

Flycatcher Muscicapa infuscata. This markedly different

composition for some flocks suggested the existence of

edge-specialist flocks. Because they were not frequent

enough in our dataset, and because we cannot exclude that

some of these different flocks are in fact subsequent

encounters with the same group of individuals, we chose to

exclude these edge-specialist flocks from further multivar-

iate analysis and to focus on the effect of edge on the typical

forest understorey flocks. The most frequent species of

these typical forest flocks can be found in Table 1. These

species were all common and conspicuous members of the

local avifauna. In summary, we identified four main kinds

of flocks: typical understorey flocks, edge-specialist flocks,

ant-following and canopy-foraging flocks. The last three

types of flocks were all rare and the following multivariate

analyses are based on 50 typical understorey flocks.

Multivariate analysis

Differences between habitats

Among the 50 flocks remaining after the outlier analysis,

MRPP revealed a strong difference between flocks sampled

in the forest interior and those sampled in the edge habitat

(P \ 0.001) with little overlap between habitats in flock

composition (Fig. 2). This result demonstrates that habitat

(edge or interior) had a major influence on mixed-species

flocks’ composition. As shown by their scores in the

multivariate analysis, some of the more edge-linked species

in the 50 flocks were Green Hylia Hylia prasina, Collared

Sunbird, Ansorge’s Greenbul Andropadus ansorgei,

Yellowbill, and Blue Cuckoo-Shrike Coracina azurea,

whereas White-throated Greenbul Phyllastrephus albigu-

laris, Brown-eared Woodpecker Campethera caroli,

Green-tailed and Common Bristlebill were amongst the

more interior linked (‘‘Appendix 2’’). A posteriori tests

(linear models) on flocks’ scores on the axes indicated that

edge effect was represented by the score on axes 1 and 3

(axis 1: r2 = 0.44, P \ 0.0001; axis 2: P = 0.08; axis 3:

r2 = 0.08, P = 0.02; axis 4: P = 0.67). Fig. 2 also illus-

trates that variance in flock composition was not smaller in

the edge flocks than in the interior (Table 2), although edge

flocks were sampled in a much smaller area.

Flock participation and species richness

Since edge and interior flocks differ in mean species

richness, we were interested in testing whether the varia-

tion in flock composition between the edge and interior

situation was mediated by or was independent from this

variation with species richness. Indeed, flock composition

significantly varied with species richness (nonparametric

MANOVA on the 50 flocks: F1,48 = 5.17, P \ 0.001;

Fig. 3): some species seemed to prefer diverse flocks (in

Table 2 Key figures about edge effect on flock structure

Habitat n Mean

richness

SD Mean score

on NMDS1

SD

Edge 27 7.0 0.5 -0.43 0.10

Interior 38 4.9 0.4 0.26 0.06

n is the sample size. Richness is the number of species in flocks.

Scores on NMDS1 represent the position of the flocks on an axis

capturing 33% of the variance in flock composition

Fig. 2 NMDS of the 50 typical understorey mixed-species flocks in

40 species space, showing edge effect. Axes 1 and 3 account for the

maximum variance (respectively, 33 and 27%) and are both related to

the effect of edge. Each dot represents one flock. Filled symbolsflocks sampled in the interior. Unfilled symbols flocks sampled in the

edge habitat

590 J Ornithol (2009) 150:585–599

123

particular Hairy-breasted Barbet Tricholaema hirsuta,

Velvet-mantled Drongo Dicrurus modestus and Blue-billed

Malimbe Malimbus nitens), whereas others associated with

few species at a time (in particular Yellow-spotted Nicator

Nicator chloris, Plain Greenbul Andropadus curvirostris

and Bates’ Paradise-Flycatcher Terpsiphone batesi). We

next checked whether variation in flock composition

between habitats was mediated by, or independent of,

variation in species richness. A posteriori tests (linear

models for edge and richness effects) on flocks’ scores on

the axes indicated no interaction between the two effects

(for the effect of species richness: axis 1: P = 0.50; axis 2:

P = 0.003; for the effect of habitat: axis 1: P = 0.03; axis

2: P = 0.53; for the interaction: axis 1: P = 0.52; axis 2:

P = 0.38). Thus, the second axis of the NMDS ordination

represented variation in flock richness independently of

edge effect (Fig. 3), while axis 1 was influenced by habitat

even when accounting for species richness.

Limited effect of species characteristics

MRPP revealed no significant effect of species’ guild on

the composition of the 50 mixed-species flocks (P = 0.43;

Fig. 4). The trend was for species to associate preferen-

tially with members of a different guild (e.g. sallying

species with searching or gleaning species), but formal test

of this hypothesis using the nearest neighbours in the

species ordinated space yielded a non-significant result

(Fisher’s exact test: P = 0.54). These results support the

alternative hypothesis that species associate independently

of their guild.

Similarly, MRPP revealed no effect of the species’

preferential feeding strata on flock participation (P =

0.20). The trend was for species to associate with species

feeding in the same strata. This trend became significant

when tested on nearest neighbours in the species ordinated

space (Fisher’s exact test: P = 0.02). However, because

the MRPP was non-significant, the support for a separate

flocking system in different strata was weak.

As expected, the a priori preference of species for edge

or interior significantly influenced flock participation (P =

0.004).

Associations between species pairs

Since habitat strongly affected species composition, we

performed interspecific association tests separately on edge

and interior flocks after having excluded outlier flocks. Only

positive associations were found: 13 out of 325 for edge

flocks (4%; Table 3) and eight out of 190 for interior flocks

(4%; Table 4). Although the frequency of significant asso-

ciations was close to the frequency predicted at random (5%,

which is the risk threshold of the test), this biased distribution

(no negative, only positive associations) suggested a non-

random mechanism. Moreover, if looking only at the core

sets of species (9 and 7 most common species in edge and

interior flocks, respectively), 20 and 19% of associations

Fig. 3 NMDS of the 50 typical understorey mixed-species flocks in

40 species space, showing effect of species richness. Axes 1 and 2

account for, respectively, 33 and 18% of the total variance and are

related to the effect of edge and species richness, respectively. Each

dot represents one flock. Filled black symbols upper quartile of flock

species richness. Unfilled symbols lower quartile of flock species

richness. Filled grey symbols flocks of medium richness

Fig. 4 NMDS of the 40 species in the 50 flocks’ space, showing

absence of guild effect. Axes 1 and 3 account for the maximum

variance (respectively, 33 and 27%). Black squares, black diamonds,

grey triangles and grey circles stand for gleaners, searchers, bark-

gleaners and salliers, respectively

J Ornithol (2009) 150:585–599 591

123

Tab

le3

Mo

difi

edC

ole

’sin

ters

pec

ific

coef

fici

ent

for

the

flo

cks

ob

serv

edat

the

edg

e

Spec

ies

GH

SU

BL

CS

ICG

RR

BD

HC

OS

UR

TG

RB

AP

FS

HD

RS

BG

RY

EL

LB

HP

FC

RM

AG

RG

RB

BM

AL

IGR

RC

MA

AN

GR

BS

WO

RC

FL

CH

WA

OL

SU

RB

HS

YE

LO

JAA

NW

BH

O

GH

SU

–0.4

2*

0.4

9*

0.3

50.4

3*

-0.0

80.3

60.5

2*

0.4

6*

0.1

00.4

00.2

10.4

00.3

40.3

40.1

20.2

80.0

10.0

10.0

10.2

80.2

80.2

80.2

10.2

1

BL

CS

––

0.4

9*

0.1

50.2

10.2

10.0

90.2

80.1

60.1

60.2

40.0

20.0

20.1

00.1

0-

0.1

50.2

1-

0.3

6-

0.0

6-

0.0

60.2

1-

0.0

60.2

10.0

5-

0.2

9

ICG

R–

––

-0.1

90.0

70.0

70.1

3-

0.0

80.4

0-

0.0

10.6

9*

0.2

80.0

60.3

70.1

40.1

4-

0.0

3-

0.3

3-

0.3

3-

0.0

3-

0.0

30.2

4-

0.0

30.0

80.4

0

RB

DH

––

––

0.7

7*

-0.3

70.3

30.1

30.2

0-

0.0

1-

0.1

90.2

80.4

9*

0.1

40.3

70.3

70.2

40.2

40.2

40.2

40.2

40.2

4-

0.0

3-

0.2

60.0

8

CO

SU

––

––

–-

0.3

10.3

8-

0.0

30.0

30.0

30.1

00.3

20.5

4*

0.4

20.4

20.4

20.0

00.2

80.2

80.0

00.0

00.2

80.0

0-

0.2

40.1

1

RT

GR

––

––

––

-0.2

60.1

80.0

30.0

3-

0.1

5-

0.1

5-

0.4

1-

0.0

8-

0.3

6-

0.3

60.0

00.0

00.0

00.0

00.0

0-

0.3

00.0

00.1

1-

0.2

4

BA

PF

––

––

––

–0.0

2-

0.1

6-

0.4

2-

0.1

00.3

80.3

80.2

20.2

20.7

10.3

20.0

30.0

30.0

3-

0.2

70.6

0*

0.0

30.1

40.1

4

SH

DR

––

––

––

––

0.0

8-

0.1

6-

0.1

0-

0.1

00.1

40.2

2-

0.0

4-

0.0

40.3

20.0

30.0

3-

0.2

70.3

20.0

30.6

0*

0.1

4-

0.2

2

SB

GR

––

––

––

––

–-

0.1

10.2

00.2

0-

0.0

60.2

70.0

00.0

00.3

7-

0.2

4-

0.2

40.0

70.3

70.0

7-

0.2

4-

0.1

90.1

7

YE

LL

––

––

––

––

––

0.2

0-

0.0

6-

0.0

6-

0.2

90.0

0-

0.2

9-

0.2

40.0

70.3

70.0

70.0

7-

0.2

40.0

7-

0.1

9-

0.1

9

BH

PF

––

––

––

––

––

–0.2

6-

0.2

90.0

50.0

50.0

5-

0.2

2-

0.2

2-

0.2

20.1

20.1

2-

0.2

20.1

2-

0.1

70.2

2

CR

MA

––

––

––

––

––

––

-0.0

10.3

30.0

50.6

1*

0.1

2-

0.2

2-

0.2

20.1

20.4

30.1

2-

0.2

20.2

20.2

2

GR

GR

––

––

––

––

––

––

–0.3

30.3

30.3

30.1

20.1

20.4

30.1

2-

0.2

20.7

40.1

20.2

20.2

2

BB

MA

––

––

––

––

––

––

––

0.1

00.4

10.1

70.1

7-

0.1

9-

0.1

9-

0.1

90.1

70.1

7-

0.1

50.2

7

LIG

R–

––

––

––

––

––

––

––

-0.2

2-

0.1

90.5

1-

0.1

9-

0.1

90.1

70.1

70.1

70.2

7-

0.1

5

RC

MA

––

––

––

––

––

––

––

––

0.1

7-

0.1

90.1

70.1

7-

0.1

90.5

1-

0.1

9-

0.1

50.2

7

AN

GR

––

––

––

––

––

––

––

––

–-

0.1

6-

0.1

6-

0.1

60.2

40.2

40.2

4-

0.1

30.3

4

BS

WO

––

––

––

-–

––

––

––

––

––

-0.1

6-

0.1

6-

0.1

6-

0.1

60.2

4-

0.1

3-

0.1

3

RC

FL

–––

––

––

––

––

––

–-

––

––

––

0.2

4-

0.1

60.2

4-

0.1

6-

0.1

3-

0.1

3

CH

WA

––

––

––

––

––

––

–-

––

––

––

–-

0.1

6-

0.1

6-

0.1

6-

0.1

3-

0.1

3

OL

SU

––

––

––

––

––

––

––

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––

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–-

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6-

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60.3

4-

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3

RB

HS

––

––

––

––

––

––

––

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––

–-

0.1

60.3

40.3

4

YE

LO

–––

––

–-

––

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–-

0.1

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3

JAA

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––

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592 J Ornithol (2009) 150:585–599

123

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J Ornithol (2009) 150:585–599 593

123

were significant (upper left part in Tables 3 and 4). In this

case, it was much higher than expected at random.

Species that were in the core sets of both edge and

interior flocks were particularly interesting for our purpose.

Icterine Greenbul was the most often involved species in

significant associations in the interior (ICGR in Table 4),

while Grey-headed Sunbird took over at the edge (GHSU

in Table 3). Except for ICGR and GHSU, few species

accumulated several positive associations. Both ICGR and

GHSU were the most frequent species in the flocks sam-

pled in interior or edge habitat, respectively. ICGR and

GHSU thus exhibited the ‘‘quantitative’’ criteria for can-

didate nucleus species, each one in a different habitat. In

both habitats, these two species were also positively asso-

ciated. Furthermore, they meet two of Moynihan’s (1962)

‘‘qualitative’’ criteria (they live in groups even when out-

side mixed-species flocks and, although not strikingly

coloured, they have conspicuous behaviour in the form of

frequent contact calls and active foraging behaviour). On

the other hand, Shining Drongo (SHDR) exhibited what we

term a ‘‘follower’’ pattern: it got involved in a single

association with the greenbul in the interior and with the

sunbird at the edge. Interestingly, the other common sal-

lying species in the interior, Black-headed Paradise-

Flycatcher, also associated with Common Bristlebill

(association BHPF–COBR in Table 3). Hence, the absence

of COBR from the edge area possibly induced the relative

scarcity of BHPF in the edge flocks. The third typical

pattern that we observed was the ‘‘independent’’ RTGR,

showing no significant association with any species, thus

suggesting no specialized interaction with other flocking

species.

Discussion

This study is, to our knowledge, the first to quantify inter-

specific bonds among participants of avian mixed-species

flocks in the Congo Basin. Similarly to most previous

studies from Asia and Africa, an active gleaning species

was found to play nucleus role, while some ‘‘sentinels’’

such as drongos Dicrurus sp. were not identified as nucleus

species by the criteria we used. They thus appear to follow

the flock, in accordance with our impressions gained from

observing the flock behaviour (G.P., unpublished data) and

with other studies (e.g. Hino 1998; Chen and Hsieh 2002)

which have similarly identified Dicrurus sp. as flock fol-

lowers. This result on drongo behaviour is clearly not valid

for every species of the genus since Dicrurus paradiseus is

an alternative flock leader in Sri Lanka (Goodale and Ko-

tagama 2006), and we cannot exclude that the presence of

D. atripennis in the flocks in our study area either enhances

flock cohesion or duration of the associations.

Compared to previous studies from the Neotropics and

tropical Asia, species richness was low, an average 5.6

species per flock. This value lies within the range reported

in South African woodlands (Thomson and Ferguson 2007)

and in Taiwan (Chen and Hsieh 2002), but at latitudes in

Asia similar to our site’s values range around 10 species

per flock (Kotagama and Goodale 2004; Lee et al. 2005)

and generally exceed 10 in South American equatorial

lowland forests (Maldonado-Coelho and Marini 2004;

Jullien and Thiollay 1998; Powell 1989; Munn and Ter-

borgh 1979), with an exceptionally high value of 21.7

reported in a montane forest in Ecuador (Poulsen 1996a).

Our low value likely results from the lower avian diversity

in the considered site than in other study areas (Weber et al.

2001), possibly linked to the recent existence of the con-

temporary African lowland forest belt as compared to other

continental rainforests. It might also reflect the fact that our

sample included temporary associations created when

mono-specific nucleus flocks entered attendants’ territories

(so-called ‘‘bird waves’’), which possibly biased the spe-

cies richness downwards. More generally, we suspect that

the flock attendance patterns were much less stable than

found in Amazonian (Munn and Terborgh 1979) and

Guianan forest (Jullien and Thiollay 1998).

Edge effect

Distance to edge, forest fragmentation and disturbance are

often critical factors in ecological community analysis.

Previous studies on avian communities of the forest un-

derstorey (Stouffer and Bierregaard 1995; Dale et al. 2000;

Maldonado-Coelho and Marini 2004; Lee et al. 2005)

showed that species assemblage varies from forest interior

to edge (or pristine to disturbed areas), either through

changes in the general frequency or in the flocking pro-

pensity of the species. Here, we obtained concordant

results in the form of an edge effect at the flock compo-

sition level. Quite intuitively, we found strong evidence

that intrinsic preference for edge or interior habitat drove

the composition of the flocks. However, the existence of

further ‘‘domino effects’’ (change in flock composition

mediated by species-specific interactions) was suggested

by the link between BHPF and COBR, which probably

induced the relative scarcity of BHPF at the edge, because

COBR is an interior specialist. In addition, the nucleus

species changed between edge (ICGR) and interior

(GHSU). Such a change from one nucleus species to the

other between different habitats within the same flocking

system has so far not been documented to our knowledge,

and might be relevant for the maintenance of flocking

behaviour in disturbed areas. Overall, the three different

edge effects documented (change in species richness,

change in the frequency of species, change in nucleus

594 J Ornithol (2009) 150:585–599

123

species) resulted in a significant difference in flock com-

position between edge and interior habitats, even if the

absence of clear-cut reaction to edge in most species (i.e.

most species were not strict habitat-specialists) and the

results of the outlier analysis showed that the edge and

interior flocks belonged to the same flocking system.

Interestingly, the three commonest flock members

(Grey-headed Sunbird, Icterine Greenbul and Shining

Drongo) are described in handbooks as avoiding degraded,

cleared forest. Here, they were found abundant in flocks

occurring at a naturally-occurring edge (Table 1), as were

to a lesser extent other interior specialists (e.g. Buff-spotted

Woodpecker). Such exploitation of edge habitats around

primary forest by specialised species (primary forest and

understorey microhabitat specialists) might be made pos-

sible by mixed-species flocking (Stouffer and Bierregaard

1995; Lee et al. 2005). Indeed, Hino (1998) suggested that

mixed-species flocking might be a way for specialised

species to broaden their ecological niche.

Two other proximal mechanisms were considered in this

study to explain the variation in flock composition between

habitats: preferential strata and species richness. If strata

were differently organised at the edge and in the interior

and strata preference influenced flock participation, this

could induce an edge effect on flock composition. We

obtained only weak support for this hypothesis; the effect

of strata was not significant in the permutation analysis.

Similarly, as flocks’ species richness varied with habitat

and influenced flock participation, it could have induced

the observed edge effect. However, we showed that both

effects were additive. Thus, the effect of edge was most

likely the result of species intrinsic habitat preference and

domino effects. Furthermore, as our data discarded the role

of exclusion of some species by others, we are not aware of

any explanation for the richness effect, which would

require confirmation through further data collection.

Evolutionary causes of flock formation

If flocking was aimed at benefiting from mutualistic

interactions between ‘‘complementary’’ species, species

from different guilds would be expected to associate

together. Yet, guilds did not play a prominent role in

species associations in our study. Our results on pair

association suggest that the general case is the lack of

mutualistic associations between flock members; most

species seem indifferent to one another when joining in a

mixed-species flock. Similarly, King and Rappole (2001)

suggest that individuals in flocks do not cooperate in food

location, and Poulsen (1996b) points that flocking is

enhanced when birds are forced to unfamiliar, risky areas.

This is also consistent with results of Pomara et al. (2007),

who showed that in several Neotropical passerine species

individuals join any flock that enter their home-range,

whatever the composition of the flock. In our case, the

behaviour of some of the flock participants (e.g. RTGR,

and most rare flock attendants) remained unexplained by

the mutualism hypothesis. For these species, intra-specific

competition and density-dependant mechanisms might

prevent or limit the formation of single-species flocks, and

mixed-species flocking might then appear as an alternative

solution to benefit from the advantages of foraging in a

large group such as reduction of predation risk (Poulsen

1996b). Such species might flock with the first nucleus

species they encounter, hence our result that the nucleus

species was the most common species in the habitat

considered.

Yet, among core species, specialised interactions

occurred; significant interactions were markedly more

common in these sets of species (they represented 19 or

20% of the possible associations in these sets of species).

‘‘Shared vigilance-foraging association’’ seemed to occur

between some species pairs (associations GHSU–SHDR in

Table 3, and ICGR–SHDR, ICGR–BHPF and COBR–

BHPF in Table 4). Recent studies showing feeding benefits

of flocking behaviour highlighted the importance of these

interactions based on the ‘‘beating effect’’ (Hino 1998;

Thomson and Ferguson 2007). Moreover, in agreement

with most studies using pair-based tests (Hutto 1994; Latta

and Wunderle 1996; King and Rappole 2000, 2001; Hart

and Freed 2003), we found only positive associations (i.e.

only species that are more often found together than

expected at random, and no species pairs that exclude each

other), and, most importantly, after having corrected for the

possible confounding effect of shared preferences for edge

or interior. These interactions (Tables 3 and 4) are possibly

mutualistic and remain to be described in more detail in

this system. The relationships between core species thus

appeared to be at least partly driven by species-specific,

habitat-dependant interactions, but mixed-species flocking

also remained largely determined by species-independent

attraction for large group size.

Zusammenfassung

Randeffekt und Struktur von gemischtartlichen

Vogelschwarmen in einem afrotropischen Tieflandwald

Gemischtartliche Vogelschwarme sind ein dominantes

Merkmal tropischer Regenwalder, und doch sind ihre Kosten-

Nutzen Bilanz und ihre Habitatabhangigkeit in Afrika nicht

vollstandig dokumentiert. Wir nahmen die Zusammensetzung

von gemischtartlichen Vogelschwarmen in einem ursprung-

lichen afrotropischen Tieflandwald in Salonga NP, DRC auf.

Unsere Daten zeigten, dass es mindestens vier Schwarmtypen

J Ornithol (2009) 150:585–599 595

123

gab, von denen einer sich auf Randhabitate spezialisierte.

Wir wandten multivariate Analysemethoden an, um den

Randeffekt auf den am haufigsten dokumentierten Typ

gemischtartlicher Vogelschwarme genauer zu charakterisi-

eren, und wir fanden einen signifikanten Effekt fur die

Schwarmzusammensetzung. Wahrend weder die okologi-

sche Gilde der Arten noch das fur den Nahrungserwerb

bevorzugte Stratum eine wichtige Rolle in der Zugehorigkeit

an einem Schwarm spielten, wurde die Schlusselrolle von

einer anderen Art am Rand und im Innern gespielt, und

sowohl die Abundanz als auch die Vergesellschaftung der

Art waren habitatabhangig, was auf einen ,,Dominoeffekt’’

auf die Struktur von gemischtartlichen Vogelschwarmen

hindeutet.

Acknowledgments G.P. thanks G. Hohmann, leader of the project

Lui Kotal, and the Max-Planck-Institute for Evolutionary Anthro-

pology for having allowed him access to the research site. We are

grateful for the helpful comments of reviewers of a previous draft of

this article.

Appendix 1

Table 5 Species seen more than once in 65 mixed-species flocks in Lui Kotal, Salonga N P. South, DRC

R E A n Edge Int Total

Musophagidae

Tauraco schuetti BBTU Black-billed Turaco 4 1 2 2 0.00 0.05 0.03

Cuculidae

Ceuthmochares aereus YELL Yellowbill 4 2 3 7 0.22 0.03 0.11

Lybiidae

Tricholaema hirsuta HBBA Hairy-breasted Barbet 4 1 2 3 0.00 0.08 0.05

Coraciidae

Eurystomus gularis BTRO Blue-throated Roller 2 2 3 5 0.15 0.03 0.08

Bucerotidae

Tockus camurus RBDH Red-billed Dwarf Hornbill 4 2 2 13 0.33 0.11 0.20

Picidae

Campethera nivosa BSWO Buff-spotted Woodpecker 3 1 2 13 0.11 0.26 0.20

Campethera caroli BEWO Brown-eared Woodpecker 3 1 2 5 0.00 0.13 0.08

Oriolidae

Oriolus brachyrhynchus WBHO Western Black-headed Oriole 4 2 2 5 0.07 0.08 0.08

Campephagidae

Coracina azurea BLCS Blue Cuckooshrike 4 2 3 11 0.37 0.03 0.17

Dicruridae

Dicrurus atripennis SHDR Shining Drongo 2 1 2 17 0.30 0.24 0.26

Dicrurus modestus VMDR Velvet-mantled Drongo 2 1 2 3 0.04 0.05 0.05

Monarchidae

Erythrocercus mccallii RCFL Red-capped Flycatcher 1 2 2 7 0.11 0.11 0.11

Terpsiphone rufiventer BHPF Black-headed Paradise-Flycatcher 2 1 2 16 0.19 0.29 0.25

Terpsiphone batesi BAPF Bates’s Paradise-Flycatcher 2 3 2 12 0.26 0.13 0.18

Platysteiridae

Diaphorophyia castanea CHWE Chestnut Wattle-eye 1 2 2 6 0.11 0.08 0.09

Prionopidae

Prionops rufiventris RBHS Rufous-bellied Helmetshrike 1 3 3 4 0.11 0.03 0.06

Muscicapidae

Stizorhina fraseri RUFT Rufous Flycatcher-Thrush 2 1 2 2 0.04 0.03 0.03

Neocossyphus rufus RTAT Red-tailed Ant-Thrush 1 1 1 2 0.00 0.05 0.03

Alethe castanea FCAL Fire-crested Alethe 1 1 1 3 0.00 0.08 0.05

Fraseria ocreata AFFF African Forest-Flycatcher 2 2 3 3 0.04 0.05 0.05

Muscicapa infuscata SOFL Sooty Flycatcher 2 3 3 3 0.11 0.00 0.05

Pycnonotidae

596 J Ornithol (2009) 150:585–599

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Appendix 2

Table 5 continued

R E A n Edge Int Total

Andropadus virens LIGR Little Greenbul 4 2 1 6 0.15 0.05 0.09

Andropadus gracilis GRGR Grey Greenbul 4 2 2 10 0.19 0.13 0.15

Andropadus ansorgei ANGR Ansorge’s Greenbul 4 2 2 4 0.11 0.03 0.06

Andropadus curvirostris PLGR Plain Greenbul 4 2 2 2 0.04 0.03 0.03

Andropadus gracilirostris SBGR Slender-billed Greenbul 4 2 3 11 0.19 0.13 0.15

Phyllastrephus albigularis WTGR White-throated Greenbul 4 1 2 3 0.00 0.08 0.05

Phyllastrephus icterinus/Phyllastrephus xavierii ICGR Icterine Greenbul/Xavier’s Greenbul 4 1 1 37 0.33 0.74 0.57

Bleda syndactyla COBR Common Bristlebill 4 1 1 8 0.00 0.21 0.12

Bleda n. notatus GTBR Green-tailed Bristlebill 4 1 1 8 0.00 0.21 0.12

Nicator chloris YSNI Yellow-spotted Nicator 4 1 1 4 0.11 0.03 0.06

Criniger calurus RTGR Red-tailed Bulbul 4 2 2 16 0.30 0.21 0.25

Sylviidae

Apalis rufogularis BTAP Buff-throated Apalis 1 2 3 4 0.11 0.03 0.06

Macrosphenus flavicans YELO Yellow Longbill 1 1 3 3 0.11 0.00 0.05

Hylia prasina GRHY Green Hylia 1 3 2 2 0.04 0.03 0.03

Timaliidae

Illadopsis fulvescens BRIL Brown Illadopsis 1 1 1 3 0.00 0.05 0.03

Nectariniidae

Deleornis axillaris GHSU Grey-headed Sunbird 1 1 2 31 0.63 0.37 0.48

Hedydipna collaris COSU Collared Sunbird 1 3 2 9 0.30 0.03 0.14

Cyanomitra olivaceus OLSU Olive Sunbird 1 1 2 4 0.11 0.03 0.06

Cynniris chloropygius OBSU Olive-bellied Sunbird 1 3 2 3 0.11 0.00 0.05

Ploceidae

Ploceus tricolor YMWE Yellow-mantled Weaver 2 2 3 2 0.04 0.03 0.03

Malimbus coronatus RCMA Red-crowned Malimbe 1 2 3 5 0.15 0.03 0.08

Malimbus cassini CAMA Cassin’s Malimbe 2 2 3 2 0.07 0.00 0.03

Malimbus nitens BBMA Blue-billed Malimbe 1 1 2 11 0.15 0.18 0.17

Malimbus malimbicus CRMA Crested Malimbe 1 1 2 8 0.19 0.08 0.12

Estrildidae

Parmoptila jamesoni JAAN Jameson’s Antpecker 1 3 2 2 0.07 0.00 0.03

Family names, scientific names, abbreviations used in Tables 2 and 3, vernacular English names, classes of feeding habits (R = 1 for leaf-

gleaning insectivores, 2 for sallying insectivores, 3 for bark-gleaning insectivores, 4 for searching insectivores), preference for edge (E = 1,2,3,

respectively for preference for interior, no preference, preference for edge), preference for a stratum (A = 1,2,3, respectively for preference for

lowest stratum below 3 m, mid stratum between 3 and 20 m and higher stratum above 20 m).

n, Edge, Int and Total refer respectively to the total number of occurrences of the species in the dataset, the frequency in the 27 edge flocks, the

frequency in the 38 interior flocks and the frequency in all 65 flocks together

Table 6 Species score in the NMDS ordination

Species NMDS1 NMDS3 Edge score

GRHY 21.437 20.197 20.616

COSU 20.927 0.807 20.474

ANGR 20.883 0.569 20.435

YELL 20.858 0.195 20.394

BLCS 20.712 0.489 20.353

GRGR -0.853 -0.503 -0.334

Table 6 continued

Species NMDS1 NMDS3 Edge score

YELO -0.571 0.614 -0.302

RBDW -0.671 -0.042 -0.292

PLGR -0.599 0.236 -0.283

RCMA -0.575 0.351 -0.282

CCFL -0.523 0.349 -0.259

JAAN -0.666 -0.433 -0.258

SBGR -0.521 -0.437 -0.193

RVPF -0.333 0.558 -0.192

BTAP -0.306 0.475 -0.174

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References

Achard F, Eva HD, Stibig HJ, Mayaux P, Gallego J, Richards T,

Malingreau JP (2002) Determination of deforestation rates of the

world’s humid tropical forests. Science 297:999–1002

Anderson MJ (2001) A new method for non-parametric multivariate

analysis of variance. Austral Ecol 26:32–46

Bearzi M (2006) California sea lions use dolphins to locate food.

J Mammal 87:606–617

Brosset A and Erard C (1986) The forest birds of North-East Gabon. I.

The species, their ecology and behaviour. Rev Ecol, Suppl 3 (in

French with English summary)

Brown CR, Brown M (1996) Social foraging 1: natural history, food

distribution and mechanisms of information transfer. Coloniality

in the Cliff Swallow. University of Chicago Press, Chicago

Chen CC, Hsieh F (2002) Composition and foraging behaviour of

mixed-species flocks led by the grey-cheeked Fulvetta in Fushan

experimental forest, Taiwan. Ibis 144:317–330

Clark CW, Mangel M (1984) Foraging and flocking strategies—

information in an uncertain environment. Am Nat 123:626–641

Cole LC (1949) The measurement of interspecific association.

Ecology 30:411–424

Dale S, Mork K, Solvang R, Plumptre AJ (2000) Edge effects on the

understorey bird community in a logged forest in Uganda.

Conserv Biol 14:265–276

Develey PF, Peres CA (2000) Resource seasonality and the structure

of mixed species bird flocks in a coastal Atlantic forest of south-

eastern Brazil. J Trop Ecol 16:33–53

Dobbs RC, Martin PR (1998) Migrant bird participation at an army ant

swarm in montane Jalisco, Mexico. Wilson Bull 110:293–295

Fruth B, Ilumbe G and Lejoly J (2003) Phytosociology for habitat

assessment in the southwestern part of Salonga National Park,

DRC. 2003 Bonobo workshop: behaviour, ecology and conser-

vation of wild bonobos. In: Thompson J, Hohmann G, Furuichi T

(eds). Inuyama, Japan, Kyoto Univ Primate Res Inst., pp 10–11

Fry CH, Keith S (2000) Picathartes to Oxpeckers: the birds of Africa,

vol 6. Academic Press, London

Fry CH, Keith S (2004) Sparrows to Buntings: the birds of Africa, vol

7. Christopher Helm, London

Fry CH, Keith S, Urban EK (1988) Parrots to Woodpeckers: the birds

of Africa, vol 3. Academic Press, London

Giraldeau LA (1984) Group foraging—the skill pool effect and

frequency-dependent learning. Am Nat 124:72–79

Goodale E, Kotagama SW (2006) Vocal mimicry by a passerine bird

attracts other species involved in mixed-species flocks. Anim

Behav 72:471–477

Hamilton WD (1971) Geometry for selfish herd. J Theor Biol 31:295–

311

Hart PJ, Freed LA (2003) Structure and dynamics of mixed-species

flocks in a Hawaiian rain forest. Auk 120:82–95

Herrera CM (1979) Ecological aspects of heterospecific flocks

formation in a Mediterranean passerine bird community. Oikos

33:85–96

Hino T (1998) Mutualistic and commensal organization of avian

mixed-species foraging flocks in a forest of western Madagascar.

J Avian Biol 29:17–24

Hohmann G and Fruth B (2003) Lui Kotal—a new site for field

research on Bonobos in the Salonga National Park. Pan Africa

News 10(2): 25–27. Available online at http://mahale.web.

infoseek.co.jp/PAN/10_2/contents.html

Hutto RL (1994) The composition and social-organization of mixed-

species flocks in a tropical deciduous forest in Western Mexico.

Condor 96:105–118

Jullien M, Clobert J (2000) The survival value of flocking in

neotropical birds: reality or fiction? Ecology 81:3416–3430

Jullien M, Thiollay JM (1998) Multi-species territoriality and

dynamic of neotropical forest understorey bird flocks. J Anim

Ecol 67:227–252

Keith S, Urban EK, Fry CH (1992) Broadbills to Chats: the birds of

Africa, vol 4. Academic Press, London

King DI, Rappole JH (2000) Winter flocking of insectivorous birds in

montane pine-oak forests in Middle America. Condor 102:664–672

King DI, Rappole JH (2001) Mixed species bird flocks in dipterocarp

forest of north central Burma (Myanmar). Ibis 143:380–390

Korb J, Salewski V (2000) Predation on swarming termites by birds.

Afr J Ecol 38:173–174

Kotagama SW, Goodale E (2004) The composition and spatial

organisation of mixed-species flocks in a Sri Lankan rainforest.

Forktail 20:63–70

Latta SC, Wunderle JM (1996) The composition and foraging ecology

of mixed-species flocks in pine forests of Hispaniola. Condor

98:595–607

Lazarus J (1979) Early warning function of flocking in birds–

experimental study with captive Quelea. Anim Behav 27:855–865

Lee TM, Soh MCK, Sodhi N, Koh LP, Lim SLH (2005) Effects of

habitat disturbance on mixed species bird flocks in a tropical

sub-montane rainforest. Biol Conserv 122:193–204

Lukoschek V and McCormick MI (2002) A review of multi-species

foraging associations in fishes and their ecological significance.

Proceedings of the 9th international coral reef symposium, pp

467–474

Table 6 continued

Species NMDS1 NMDS3 Edge score

GHSU -0.401 -0.083 -0.170

YMWE -0.509 -1.174 -0.128

RBHS -0.198 0.002 -0.087

WBHO -0.133 0.345 -0.087

LIGR -0.083 0.438 -0.072

CRMA -0.1 0.324 -0.071

EOSU 0.06 0.121 0.016

RTGR 0.109 0.214 0.030

BBTU 0.02 -0.628 0.060

VMDR 0.192 0.085 0.078

RTAT 0.286 0.105 0.117

SHDR 0.286 0.07 0.120

CHWA 0.344 0.269 0.129

ICGR 0.339 0.036 0.146

HBBA 0.174 -0.901 0.150

BHPF 0.396 0.013 0.173

GRMA 0.38 -0.244 0.187

BFWO 0.434 -0.171 0.205

GTBR 0.551 20.888 0.315

COBR 0.651 20.481 0.326

BEWO 0.811 0.32 0.331

WTGR 0.766 20.556 0.383

Edge score is the combination of the species score on NMDS1 and

NMDS3 that accounts for the correlation between these axes and the

habitat variable. The more negative the edge score, the more edge-

linked the species. See ‘‘Appendix 1’’ for full species names.Species

mentioned in the main text as being the most edge/interior linked are

shown in bold

598 J Ornithol (2009) 150:585–599

123

Maldonado-Coelho M, Marini MA (2004) Mixed-species bird flocks

from Brazilian Atlantic forest: the effects of forest fragmentation

and seasonality on their size, richness and stability. Biol Conserv

116:19–26

Maurer BA (1984) Interference and exploitation in bird communities.

Wilson Bull 96:380–395

McCune B, Grace JB (2002) Analysis of ecological communities.

Mjm Software Design, OR

Mielke PW, Berry KJ (2001) Permutation methods: distance function

approach. Springer Series in Statistics. New York, USA

Morse DH (1970) Ecological aspects of some mixed-species foraging

flocks of birds. Ecol Monogr 40:119–168

Moynihan M (1962) The organisation and probable evolution of some

mixed-species flocks of Neotropical birds. Smithsonian Miscel-

laneous Collections 1437

Munn CA (1986) Birds that cry wolf. Nature 319:143–145

Munn CA, Terborgh JW (1979) Multispecies territoriality in

Neotropical foraging flocks. Condor 81:338–347

Nemeth Z, Moore FR (2007) Unfamiliar stopover sites and the value

of social information during migration. J Ornithol 148(Suppl.

2):S369–S376

Oksanen J, Kindt R, Legendre P, O’Hara B, Henry M, Stevens H (2007)

vegan: Community Ecology Package. R package version 1.8–8.

http://cran.r-project.org/, http://r-forge.r-project.org/projects/vegan/

Pomara LY, Cooper RJ, Petit LJ (2007) Modelling the flocking

propensity of passerine birds in two Neotropical habitats.

Oecologia 153:121–133

Poulsen BO (1996a) Structure, dynamics and home-range of two mixed

species flocks and species composition in a montane Alder

dominated secondary forest in Ecuador. J Trop Ecol 12:333–343

Poulsen BO (1996b) Relationships between frequency of mixed-

species of mixed-species flocks, weather and insect activity in a

montane cloud forest, Ecuador. Ibis 138:466–470

Powell GVN (1989) On the possible contribution of mixed species

flocks to species richness in Neotropical avifaunas. Behav Ecol

Sociobiol 24:387–393

R Development Core Team (2005) R: A language and environment for

statistical computing. R Foundation for Statistical Computing,

Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org

Stensland E, Angerbjorn A, Berggren P (2003) Mixed species groups

in mammals. Mammal Rev 33:205–223

Stouffer PC, Bierregaard RO (1995) Use of Amazonian forest

fragments by understory insectivorous birds. Ecology 76:2429–

2445

Stratford JA, Stouffer PC (1999) Local extinctions of terrestrial

insectivorous birds in a fragmented landscape near Manaus,

Brazil. Conserv Biol 13:1416–1423

Tabachnik BG, Fidell LS (1989) Using multivariate statistics. Allyn

& Bacon, New York

Thiollay JM (1999) Frequency of mixed species flocking in tropical

forest birds and correlates of predation risk: an intertropical

comparison. J Avian Biol 30:282–294

Thomson RL, Ferguson JWH (2007) Composition and foraging

behaviour of mixed-species flocks in two adjacent African

woodland habitats: a spatial and temporal perspective. Ostrich

78(1):65–73

Urban EK, Fry CH, Keith S (1997) Thrushes to Puffbacks,

Flycatchers: the birds of Africa, vol 5. Academic Press, London

Waite TA, Grubb TC (1988) Copying of foraging locations in mixed-

species flocks of temperate-deciduous woodland birds—an

experimental study. Condor 90:132–140

Weber W, White L, Naughton-Treves L, Vedder A (eds) (2001)

African rain forest ecology and conservation: an interdisciplinary

perspective. Yale University Press, New Haven

J Ornithol (2009) 150:585–599 599

123