Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 February 2021 | 13(2): 17646–17650
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
https://doi.org/10.11609/jott.6374.13.2.17646-17650
#6374 | Received 08 July 2020 | Final
received 09 February 2021 | Finally accepted 15 February 2021
Foraging behavior and association
with mixed flocks by the Critically Endangered Alagoas Tyrannulet Phylloscartes ceciliae
(Aves: Passeriformes: Tyrannidae)
Carlos Otávio
Araujo Gussoni 1 & Tatiana Pongiluppi
2
1 Rua 12B,
621, Vila Indaiá, Rio Claro, SP, 13506-746, Brazil.
2 Brazil
Birding Experts. Rua Joãozito Arruda, 2180,
Parque Iracema, Fortaleza, CE, 60824-075, Brazil.
1 cogussoni@gmail.com
(corresponding author), 2 tatianapongiluppi@gmail.com
Editor: Anonymity requested. Date
of publication: 26 February 2021 (online & print)
Citation: Gussoni, C.O.A. & T. Pongiluppi
(2021). Foraging behavior and association with mixed
flocks by the Critically Endangered Alagoas Tyrannulet Phylloscartes
ceciliae (Aves: Passeriformes: Tyrannidae). Journal of Threatened Taxa 13(2): 17646–17650. https://doi.org/10.11609/jott.6374.13.2.17646-17650
Copyright: © Gussoni & Pongiluppi 2021. Creative Commons Attribution 4.0 International
License. JoTT
allows unrestricted use, reproduction, and distribution of this article in any
medium by providing adequate credit to the author(s) and the source of publication.
Funding: Aage V. Jensen Charity Foundation, Marshall-Reynolds Foundation, American
Bird Conservancy (ABC), WWF-Brasil, Mohamed Bin Zayed Species Conservation Fund, Conservation Leadership Programme, SOS Mata Atlântica,
Ricoh Co. Ltd., BirdLife International,
Fundação Grupo Boticário de Proteção à Natureza, Albert and Nancy Boggess.
Competing interests: The authors declare no competing interests.
Author details: Carlos Gussoni is an ornithologist who holds a PhD in Zoology. He
has worked with the natural history of the Restinga
Tyrannulet for almost 10 years. Tatiana Pongiluppi is birdwatching guide at Brazil Birding
Experts.
Author contribution: COAG and TP collected the data in the field and wrote
the article.
Acknowledgements: We are grateful to P.F. Develey
and the SAVE Brasil team for the aid provided during
fieldwork in Serra do Urubu Mountains, and especially to J.A.V. Filho, the
guardian of this important forest that supported us the whole time. To M.C. Vieira, P.R. Anunciação,
and P.F. Develey for their helpful comments on the
manuscript. The Aage
V. Jensen Charity Foundation, Marshall-Reynolds Foundation, American Bird
Conservancy (ABC), WWF-Brasil, Mohamed Bin Zayed
Species Conservation Fund, Conservation Leadership Programme,
SOS Mata Atlântica, Ricoh Co. Ltd., BirdLife International, Fundação
Grupo Boticário de Proteção
à Natureza, Albert and Nancy Boggess provided
financial support.
Abstract: The Alagoas Tyrannulet Phylloscartes ceciliae
is a Critically Endangered species with a restricted distribution to the
Atlantic Forest of the Pernambuco Endemism Center. It seems to specialize in using the
sally-strike maneuver (68.85%) to catch prey on green foliage (50.82%) and in
the air (34.42%). We calculated a catch
rate of 2.93 catches/minute, identified a new food item for this species
(caterpillars), and included 12 species in the list of birds recorded in mixed
flocks with the species. Our results
show that majority of the prey capture events by Alagoas Tyrannulet occurred
inside tree canopies, thus we can infer that this species needs a more advanced
stage of forest sucession, with higher trees,
emphasizing the urgency for restoration programs in the region.
Keywords: Atlantic forests, endemic bird,
Serra do Urubu, threatened species.
Resumo: O cara-pintada
(Phylloscartes ceciliae)
é uma espécie criticamente ameaçada de extinção com distribuição restrita à Mata Atlântica do
Centro de Endemismo Pernambuco. Utiliza preferencialmente a manobra investir-atingir (68,85%) para capturar
presas em folhas verdes (50,82%) e no ar (34,42%). Captura em média
2,93 presas/minuto, incluindo lagartas de Lepidoptera
(novo item alimentar registrado
para a espécie).
Registramos doze novas
espécies na lista de aves presentes
em bandos mistos com P. ceciliae.
Nossos resultados mostraram que a espécie forrageia preferencialmente no
interior das copas de árvores,
necessitando de florestas em estágio sucessional
avançado, com árvores altas, sendo urgentes
ações de restauração em sua área
de ocorrência.
Introduction
Alagoas Tyrannulet Phylloscartes
ceciliae (Image 1) is a globally threatened
species (Critically Endangered; BirdLife
International 2020) with a restricted distribution to the Pernambuco Endemism
Center (Roda et al. 2011). This bird is found in 13 municipalities in
the states of Alagoas and Pernambuco, however within only five protected areas
(Roda et al. 2003; BirdLife
International 2020; GBIF 2020; WikiAves 2020). Data on this species biology are still
scarce. There is only sparse information
about the species (e.g., Teixeira 1987; Collar et al. 1992; Roda et al. 2011).
Here, we provide the first detailed information about the foraging
behavior of P. ceciliae and new
information about association with mixed flocks.------
Materials and Methods
Study area. We collected field data mainly in 2009 in Frei Caneca, and Pedra D’Antas Private Reserves (RPPNs) which encompass 1,066ha of
protected area, both located at Serra do Urubu Mountains (-8.717S, -35.840W),
in Jaqueira and Lagoa dos
Gatos municipalities, Pernambuco, northeastern Brazil. The Serra do Urubu Forest Complex is one of
the largest remaining areas of montane forest in the state of Pernambuco. Located in a region known as Pernambuco
Endemism Center, Serra do Urubu is classified by the Brazilian Ministry of
Environment as an area of extreme biological importance and identified by BirdLife International and SAVE Brasil
as an Important Bird and Biodiversity Area (IBA) of high priority action. The predominant vegetation is montane dense ombrophilous forest based on the types of vegetation
proposed by Veloso (1992) and the altitude varies from 600 to 750 m. We also recorded some information about
associations of P. ceciliae with mixed flocks
between 2010 and 2015. This study is
part of the bird monitoring program of Serra do Urubu, conducted annually since
2005.
We actively searched for individuals of P. ceciliae from 18–27 November 2009, mainly during
05.00–08.00 h and 16.00–18.00 h, to collect information about the species’
foraging behavior. We used the
focal-animal method (Altmann 1974; Martin & Bateson 1986) following
individuals as long as possible and observing their foraging strategies with
10x binoculars. The interval between
each observation was five minutes long so that they could be considered as
independent samples (according to Alves & Duarte 1996). Any attempt of capture was treated as a
sample of foraging behavior, either it was a successful attempt or not, as
proposed by Fitzpatrick (1980). We
classified the maneuvers according to Remsen & Robinson (1990). Also, we recorded the following parameters
for each capture: substrate type (tree, shrub, or herbaceous), substrate
characteristics (the presence and type, simple or pinnate, of the green leaves,
dry leaves and/or twigs), substrate height, bird position on the substrate
(inside/outside the canopy), the site where capture began (features: branches
with green/dry leaves or twigs; height; and slope: horizontal = any angle
between 0 and 15°, tilt = between 16 ° and 70°, vertical = between 71° and
90°), the site where capture ended (features: branches
with green/dry leaves or twigs; height, and slope), the substrate where the
prey was captured (air, green foliage, dry foliage, branch, stem,
inflorescence; height), the distance between the start and the return perches,
the distance from the bird to the prey, the distance from the prey to the new
resting place (estimated visually), the height of the site where the prey lay,
prey identity (when possible), whether the bird returned or not to the perch of
departure, and the maneuver performed to capture. In addition, for aerial maneuvers, we
recorded flight slope and direction.
Other information on the biology of the species was collected ad libitum
(Altmann 1974). The total dataset
consisted of 61 foraging samples.
Results
Foraging behavior
The Alagoas Tyrannulet seems to specialize in using
the sally-strike maneuver (68.85%; n= 61) to catch prey (n= 61) on green
foliage (50.82%) and in the air (34.42%).
P. ceciliae used mainly branches
with green leaves as both starting (68.86%) and return perches (70.49%). The other maneuvers used to catch prey were:
reach-up (4.92%), reach-out (13.11%), lunge (4.92%), sally-hover (6.56%), and
glean (1.64%). Individuals also captured
prey on dry leaves (6.56%), dry branches (4.92%), inflorescences (1.64%), and
trunks (1.64%). Among the prey capture
substrates, P. ceciliae preferred small
pinnate leaves, which accounted for 32.72% of the catch substrates, while
simple leaves corresponded to 24.59%.
The main prey manipulation (n= 61) performed was engulfing (93.44%),
followed by gulping (3.28%), beating prey against dry branches (1.64%), and
deliverance to another individual (1.64%).
The species also foraged either alone or in pairs,
mainly in trees with green leaves (81.97%) 18.10 ± 6.03m high (median= 18m;
min.= 8m; max.= 30m), with most capture events occurring inside tree canopies
(98.36%). Individuals preferentially
used tilted branches as perches of departure (75.41%) and return (70.49%), with
the perches of departure being 12 ± 5.36 m high (median= 13.95m; min.= 5m;
max.= 25m) and return perches were at 12 ± 5.21 m above ground (median= 13.86m;
min.= 5m; max.= 25m). Most flights were
also slanted (58.33%), with 64.41% out of them being slanted up while 16.95%
were slanted down. On the other hand,
16.95% of flights were horizontal flights, and 1.69% were vertical-up
ones. In none of the aerial maneuvers
observed did the birds return to the perch after catching the prey. The distance from the initial perch to the
return one ranged from 0 to 3.3 m (median= 54.32cm; mean= 50 ± 54.39cm), the
distance from the bird to the prey ranged from 2cm to 1m (median= 29.61cm;
mean= 30 ± 20.53cm) and the distance from the prey to the new perch ranged from
0 to 3 m (median= 35.68cm; mean= 30 ± 45.09cm).
Phylloscartes ceciliae’s successful
catch rate was 2.93 catches/minute. In
two capture events, it was possible to identify the prey: two caterpillars of
approximately 5mm long each. One of them
was captured by one individual and delivered to another one on the return perch
(25 November 2009). In November 2009, we
observed three individuals foraging together, possibly a family group.
Association with mixed flocks
We observed four events in which individuals of
Alagoas Tyrannulet accompanied mixed flocks in July (n= 1), November (n= 2),
and December (n= 1). The mixed flocks
were composed of the following species (the number of flocks in which they are
present are in brackets): Myrmotherula axillaris (n= 3), Terenura
sicki (n= 2), Dysithamnus
mentalis (n= 1), Herpsilochmus atricapillus (n= 1), Ceratopipra
rubrocapilla (n= 1), Tolmomyias
flaviventris (n= 1), Cyclarhis
gujanensis (n= 1), Basileuterus
culicivorus (n= 1), Coereba
flaveola (n= 1), Saltator
maximus (n= 1), Tachyphonus rufus (n= 1), Tangara
cayana (n= 1), Dacnis
cayana (n= 1), Hemithraupis
guira (n= 2), and Euphonia violacea
(n= 1). In November 2009, contacts
with the other species in mixed flocks corresponded to only 4.54% of the
sightings of P. ceciliae (n=
44), indicating that this species is not a frequent follower of these flocks.
Discussion
Foraging behavior
The data obtained added new information about the
foraging activity of P. ceciliae,
allowing a more detailed description of the strategies used by this species to
catch prey. According to Teixeira
(1987), P. ceciliae forage on the
surface of leaves and branches, where it catches small insects. Collar et al. (1992) reported that
this species feeds 6–15 m above ground level, capturing its prey with rapid
movements directed to the axial and abaxial leave surfaces.
The foraging height we observed in the current study
agrees with other reports for species in the genus Phylloscartes,
which forage from the lower stratum to the forest canopy where they inhabit (Narosky & Yzurieta 1987;
Parker III 1992; Ridgely & Tudor 1994; Willis & Oniki
2003; Fitzpatrick et al. 2004; Sigrist 2005;
Maldonado-Coelho 2009). As reported
herein, several other species of the genus forage alone, in pairs or small
groups, including family groups (Collar et al. 1992; Ridgely & Tudor 1994;
Fitzpatrick et al. 2004; Birdlife International 2009). Many species of Phylloscartes
often catch prey on leaves and/or in the air (see Fitzpatrick et al.
2004). Moreover, the Alagoas Tyrannulet
seems to have a preference for capturing prey from small pinnate leaves, as
reported by Maldonado-Coelho (2009) for P. roquettei.
Collar et al. (1992) recorded the capture of a
tettigoniid (Orthoptera) by an individual of P. ceciliae,
and Teixeira (1987) reports that this bird feeds on small insects. In this study, we report a new food item on P.
ceciliae’s diet: caterpillars. This item is also present in the diet of
other species such as P. kronei (Gussoni & Santos 2011), P. ventralis
(Smith & Betuel 2006), P. eximius (Belton 1994), and P. oustaleti
(Gonzaga et al. 2016). The catch
rate is similar to that found for P. kronei
that catches, on average, 2.12 prey/min (Gussoni
& Santos 2011).
Association with mixed flocks
According to Fitzpatrick et al. (2004), all
species of the genus Phylloscartes accompany
mixed bird flocks, however, it is not clear which bird species are associated
with Phylloscartes species in these
groups. Literature reports the presence
of species from at least 12 families within mixed flocks with Phylloscartes (Teixeira 1987; Collar et al. 1992;
Parker III 1992; Gonzaga & Pacheco 1995; O’Neill et al. 2000; Willis & Oniki 2003; Fitzpatrick et al. 2004; Venturini et al. 2005; Bodrati
& Cockle 2006; O’Shea et al. 2007; Santos et al. 2009). Teixeira (1987) and Roda
et al. (2003) found 19 species in mixed bird flocks with P. ceciliae. The
current study included 12 new species to the list, totaling 31 species recorded
in flocks with the species. As described
for P. kronei by Gussoni
(2010), P. ceciliae is not a frequent
follower of mixed bird flocks. Other
species of Phylloscartes, however, may follow
such aggregations more often. P. ventralis, for example, is regurlarly
found among mixed bird flocks, being recorded in 13% of the flocks studied by Ghizoni-Jr. (2009) in Santa Catarina.
The natural history data presented here is valuable to
support conservation efforts and possible management actions for this
species. It is well known that other
species are locally extinct in our study area and two of them are probably
extinct in the wild, the Alagoas Foliage-gleaner Philydor
novaesi and the Cryptic Treehunter
Cichlocolaptes mazarbarnetti,
and others are on the brink of extinction such as the Alagoas Antwren (Myrmotherula snowi; known mainly for one site, Murici
Ecological Station, nowadays).
Unfortunately, the Alagoas Tyrannulet is one of the next candidates to
require a recovery plan and our findings are useful for the conservation practioners to design the best management strategies. Also, our results show that the majority of
the prey capture events by Alagoas Tyrannulet occurred inside tree canopies,
thus we can infer that this species needs a more advanced stage of forest sucession, with higher trees, emphasizing the urgency for
restoration programs in the region.
Fortunately, there are some actions led by the NGO SAVE Brasil to recover the habitat and bring some hope for these
birds on the brink of extinction at Serra do Urubu.
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