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Universidade Federal do Rio Grande do Norte
Centro de Biociências
Programa de Pós-graduação em Psicobiologia
COMPORTAMENTO SOCIAL E TERRITORIALIDADE
ALIMENTAR NA GARÇA-AZUL, Egretta caerulea (L.)
EMMANUEL MORALEZ DA SILVA
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EMMANUEL MORALEZ DA SILVA
COMPORTAMENTO SOCIAL E TERRITORIALIDADE ALIMENTAR NA GARÇA-
AZUL, Egretta caerulea (L.)
Dissertação apresentada à Universidade
Federal do Rio Grande do Norte, para
obtenção do título de Mestre em
Psicobiologia.
Orientador: Flávio José de Lima Silva
Natal
2008
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Título: COMPORTAMENTO SOCIAL E TERRITORIALIDADE ALIMENTAR NA
GARÇA-AZUL, Egretta caerulea (L.)
Autor: EMMANUEL MORALEZ DA SILVA
Data da defesa: 28 de março de 2008.
Banca Examinadora:
___________________________________
Profa. Celine de Melo
Universidade Federal de Uberlândia, MG
___________________________________
Prof. Arrilton Araújo
Universidade Federal do Rio Grande do Norte, RN
___________________________________
Prof. Flávio José da Lima Silva
Universidade Federal do Rio Grande do Norte, RN
“When we submerge into the divine, the events of yesterday - that once seemed so important
to us - no longer exist, and tomorrow no longer hides in the mystery. All reasons to regret the
past or worrying about the future dissolve in the perpetual and sweet contact with the divine
and always renewed joy of the Spirit - the Eternal Present, the only Reality.”
Paramahansa Yogananda
Agradecimentos
Agradeço a:
( V ) Deus;
( V ) Família;
( V ) Amigos;
( V ) Demais.
Resumo
A utilização do habitat é parte importante da biologia de uma espécie. Um dos
recursos importantes para a sobrevivência e reprodução de um indivíduo é o recurso
alimentar. Desta forma, as interações sociais que um animal mantém durante as atividades de
forrageio são de suma importância dentre seus aspectos comportamentais, os quais, por sua
vez, representam a parte de um organismo através da qual este interage com o ambiente,
adaptando-se as variações e mudanças no meio. Garças são conhecidas por formar agregações
alimentares que podem conter até milhares de indivíduos, nas quais componentes sociais do
forrageio têm sido identificados e estudados para várias espécies. Estudos mais aprofundados
destes aspectos ainda são escassos para a garça-azul, Egretta caerulea. Desta forma, o
objetivo deste estudo foi descrever o comportamento social (posturas de exibição,
vocalizações e interações co-específicas) e a territorialidade da espécie durante o período de
forrageio em uma área de baixio lodoso no sistema estuarino de Cananéia, litoral sul do
estado de São Paulo, Brasil. Observou-se a defesa de uma área fixa e exclusiva, próxima ao
manguezal, através da expulsão; algo que ainda não tinha sido registrado com dados concretos
para a espécie. Registraram-se taxas de captura e sucesso maiores para indivíduos forrageando
na área correspondente ao território defendido, assim como menores taxas de investimento no
forrageio. Desta forma, esta pode ser uma das razões pelo estabelecimento de territórios pela
espécie no local. Registraram-se quatro posturas de exibição para a espécie, das quais duas
são novas na literatura e são utilizadas nas interações entre indivíduos. Registrou-se uma
vocalização, que aparentemente é importante no contexto social do forrageio para a espécie e,
possivelmente, tem função de advertência e proclamação da posição de dominância ocupada
pelo indivíduo territorial dentro do grupo. Um indivíduo territorial utiliza-se de três
comportamentos, dos descritos: expulsão, vocalização e encontro (encontro agonístico entre
indivíduos, sem agressão física). Destes, aparentemente a expulsão é utilizada na defesa ativa;
enquanto que os outros dois comportamentos são utilizados de uma forma mais passiva, na
manutenção da posição de dominância do indivíduo, ajudando-o na defesa de seu território de
uma forma menos direta. Assim, com os resultados apresentados neste trabalho,
identificaram-se novos componentes do comportamento social da utilização do recurso
alimentar pela garça-azul, incorporando-se aspectos do comportamento territorial para um
futuro entendimento de sua possível significância adaptativa. Reforça-se também a
importância das interações sociais de garças que forrageiam em agregados contendo milhares
de indivíduos, em áreas ecologicamente importantes.
Palavras-chave: Comportamento Territorial, Defesa, Estuário, Garça-azul, Posturas de
exibição, Território.
- 7 -
Abstract
The use of habitat is an important part of a species biology. One resource of great
importance for the survivor and reproduction of an individual is the food resource. Thus, the
social interactions an animal has during the feeding activities are of extremely importance
within its behavioral aspects, which represents the part of an organism trough which it
interacts with the environment, adapting to changes and variations. Herons are known to form
feeding aggregations of even more than thousands of individuals, in which social components
of foraging have been identified and studied for several species. More profound studies of
these aspects are yet to poor for the Little Blue Heron, Egretta caerulea. Therefore, the aim of
this study was to describe the social behavior (display postures, vocalizations and co-specific
interactions) and the territoriality of the specie during the feeding period in an area of mud
bank in the estuarine system of Cananéia, south coast of São Paulo state, Brazil. The defense
of a fixed and exclusive area, closest to the mangrove, trough expulsion was observed; some
thing that have not yet been registered with concrete data for the specie. Higher capture and
success rates, and lower investment rates (steps/min and stabs/min) were registered for
individuals foraging in areas corresponding to the defended territory. This could be one of
possible reasons for the establishment of territories in the area. Four display postures were
registered for the specie, two of then new in the literature, which are used in the interactions
between individuals; one vocalization, that apparently is important in the social context of
foraging for the specie and, possibly, has a function of advertising and proclaiming the
dominance position of the territorial individual within the group. A territorial individual uses
three behaviors, of the ones described: expulsion, vocalization and encounter (agonistic
encounter between individuals, without physical aggression). Of these, the expulsion is
apparently used in the actual defense, actively; while the other two behaviors are used in a
more passive way, in the maintenance of the dominance position of the individual, helping it
in the defense of its territory in a less direct manner. Therefore, with the results presented in
here, new components of the social utilization of the feeding resource for the Little Blue
Heron were identified, incorporating aspects of the territorial behavior for a future
understanding of its possible adaptive significance. And it also reinforces the importance of
the social interactions of herons foraging in great aggregations, in areas ecologically
important.
Key-words: Defense, Display postures, Estuary, Little Blue Heron, Territory, Territorial
behavior.
Sumário
Resumo
vi.
Abstract viii.
Introdução Geral 10.
Objetivos do estudo 14.
Manuscrito 1 - Territorialidade Alimentar na garça-azul, Egretta caerulea, em
Cananéia, Brasil 15.
Manuscrito 2 - Comportamento Social de Garças–azuis, ao Forrageio, no Sudeste do
Brasil 44.
Manuscrito 3 - Comportamento Territorial da Garça-azul, Egretta caerulea 69.
Discussão/Conclusão Geral 96.
Bibliografia Citada na Introdução e Discussão/Conclusão Geral 100.
10
Introdução Geral
O estudo do comportamento animal é uma ponte entre os aspectos moleculares e
fisiológicos da biologia e da ecologia. O comportamento é a ligação entre organismos e o
ambiente, e entre o sistema nervoso e o ecossistema. É uma das propriedades mais
importantes da vida animal e tem um papel fundamental nas adaptações das funções
biológicas. (Snowdon 1999). Snowdon demonstra por alguns ângulos a importância do
entendimento do comportamento de um organismo, grupo, espécie, no estudo de sua biologia.
Desta forma, o presente estudo vem contribuir para um melhor conhecimento da biologia de
uma espécie tão importante quanto todas as outras existentes, agora ou no passado.
Um indivíduo pode apresentar comportamentos dirigidos a si mesmo, ou
comportamentos dirigidos a outros indivíduos, sejam estes da mesma espécie ou não, podendo
estes também ser de diversas naturezas. Assim, pode-se dizer que este indivíduo está engajado
em uma interação social. Porém, o termo social nem sempre foi empregado a indivíduos
simplesmente interagindo entre si. Distinção entre grupos sociais e agregações foi tema de
discussão durante algum tempo entre etólogos e ecólogos. Os etólogos acreditavam que
grupos sociais formavam-se pela genuína atração entre indivíduos, enquanto que agregações
eram meramente coincidências estatísticas de indivíduos convergindo para um mesmo recurso
(Giraldeau & Caraco 2000). Já os ecólogos propuseram uma distinção em nível funcional:
grupos sociais são compostos por indivíduos que tem vantagens evolutivas pela presença de
outros, enquanto que agregações não (Giraldeau & Caraco 2000). Hoje em dia o termo social
é empregado de uma forma mais abrangente; e o conceito utilizado por Giraldeau & Caraco
(2000), o qual aponta social como sendo qualquer conjunto de indivíduos que podem ser
ligados por relações mutuas, é adotado aqui para compreender as interações alimentares da
espécie estudada.
Garças são conhecidas por formar agregações alimentares de altas densidades em
áreas de grande disponibilidade de presas (Kushlan 1981). Várias características sociais destas
agregações já foram estudadas, quanto a sua formação, estrutura e dinâmica. A formação está
ligada à atração das várias espécies pelas espécies brancas (locais nos quais indivíduos
brancos estão presentes atraem mais indivíduos que estejam procurando locais de
alimentação), especialmente a garça-branca-pequena (Egretta thula) (Simth 1995, Caldwell
1981, Kushlan 1977), assim como também pela utilização da informação disponível, na
colônia, das aves que vão e voltam das áreas alimentares - teoria do “centro de informação”
(Ward & Zahavi 1973) - (Erwin 1983, Pratt 1980, Custer & Osborn 1978, Krebs 1974,1978).
11
As agregações podem ser mono-específicas ou conter várias espécies, as quais podem se
diferenciar quanto ao tamanho, morfologia de bico, comportamento alimentar e também
ocupar as agregações em tempos variados, levando-as a diferentes formas de ocupação e
utilização dos recursos em uma mesma área (Battley et al. 2003, Master 1992, Kersten et al.
1991, Kushlan et al. 1985, Erwin 1983, Kushlan 1976b). Estas agregações podem trazer
benefícios alimentares para os indivíduos, como o aumento das taxas de captura e sucesso
(Smith 1995, Master et al. 1993, Götmark et al. 1986, Krebs 1974). Custos também podem
estar associados a estas grandes concentrações de indivíduos, como o aumento na competição
por recursos, o aumento da evidência em relação a predadores e o aumento de doenças e
transmissão parasitária como resultado da proximidade entre os indivíduos (Alcock 2005,
Krebs & Davis 1997). Desta forma, estas convergências de indivíduos para a mesma área não
são ao acaso, e os indivíduos envolvidos desenvolvem relações mutuas que afetam uns aos
outros de forma específica.
A seleção e a utilização do habitat são importantes dentro da biologia de uma espécie,
podendo levar a conseqüências que atuam diretamente nas interações entre espécies e
indivíduos em uma comunidade, assim como em uma determinada área alimentar (Morin
1999). Desta forma, quando indivíduos forrageiam juntos, em uma mesma área e utilizando-se
dos mesmos recursos, pode haver uma sobreposição de nicho entre eles; e ambos acabam por
buscar os mesmos recursos e uma competição pode se estabelecer.
Diferentes formas de competição são reconhecidas (Ricklefs 2001, Krebs & Davis
1997). Na forma mais simples, a exploração, ambos os indivíduos predam sobre o mesmo
recurso, diminuindo as chances de sucesso de cada um; em outra forma os indivíduos tentam
ser o mais rápido na captura da mesma presa, porém sem agressão (“scramble”); e na disputa
direta, os indivíduos interagem agressivamente para capturar o recurso (Milinski & Parker
1991). Uma das formas de utilização do recurso é pela defesa deste, levando a uma
distribuição despótica, na qual poucos indivíduos excluem os outros de uma área rica em
recursos (Krebs & Davis 1997).
Assim, o comportamento social de uma espécie está intimamente relacionado ao seu
comportamento de forrageio, determinando suas tendências nas interações durante o período
alimentar e, por conseqüência, influenciando na utilização do habitat pela espécie. Desta
forma, tornam-se interligados o comportamento social e a utilização despótica do recurso
alimentar.
Território é um espaço fixo, do qual um indivíduo ou grupo de indivíduos mutuamente
tolerantes excluem potenciais exploradores de um determinado recurso ou recursos (Maher &
12
Lott 1995). Para manter este território, o indivíduo necessita utilizar-se de comportamentos
específicos, relacionados à defesa territorial e que transmitam ao oponente a mensagem
específica. Tais comportamentos podem agir de forma ativa ou passiva no oponente. A forma
ativa de defesa é pela perseguição e luta, contato físico agressivo entre os indivíduos (Hoem
et al. 2007, Sogge et al. 2007, Oliver et al. 2006, Moulton et al. 2004, Gese 2001, Turner
1994); de uma forma mais sucinta, os indivíduos podem manter áreas exclusivas mandando
sinais como cheiros através da urina, das fezes ou de substancias produzidas em glândulas
especializadas (Mertl-Millhollen 2006, Barja et al. 2005, Gautier et al. 2004, Shelly 2004,
Gautier & Miaud 2003, Blanchard et al. 2001, Sillero-Zubiri & Macdonald 1998, Peters &
Mech 1975), cantos ou vocalizações (Ripmeester et al. 2007, Searcy et al. 2006, Aubin et al.
2004, Bee & Gerhardt 2002, Jaeger et al. 1996, Kroodsma & Byers 1991) ou exibições
sinalizando ameaça (Kohn et al. 2005, Markus 2002, Gese 2001, Savalli 1993, Schwab &
Stout 1991, Simpson 1968); aspectos estes revisados em Stamps 1994 e Davis & Houston
1984.
Diferentes espécies de aves apresentam comportamento de defesa territorial fora do
período reprodutivo, defendendo uma porção de área que contém o recurso alimentar. Estes
territórios são considerados territórios de inverno, ou tipo E (Wilson 1975, Nice 1941). Entre
as espécies que tiveram este tipo de territorialidade registrado, temos vários Passeriformes
(Koronkiewicz et al. 2006, Brotons 2000, George 1987, Lederer 1977, Daves 1976),
diferentes espécies de aves marinhas (Trippi & Collazo 1997, Turpie 1995, Mayers et al.
1979), entre outras. Dentre os Ciconiiformes, apenas a Egretta garzeta (Nota 2003, Yamada
1994), a Egretta sacra (Recher 1972) e a Ardea cinerea (Marion 1989, Richner 1986) tiveram
territórios de inverno registrados.
A garça-azul, Egretta caerulea (L.), é uma espécie de garça com ampla distribuição no
continente americano, tendo na América do Sul sua ocorrência bastante ligada às áreas
costeiras, especialmente sistemas marinho/estuarinos (Sick 1997), como o Complexo
Estuarino Lagunar de Iguape-Cananéia (sul do estado de São Paulo), nos quais é uma espécie
bastante numerosa. No Hemisfério Norte, vários aspectos de sua biologia foram estudados,
desde os anos 40, por diversos autores. Aspectos ecológicos têm sido os mais abordados
durante os anos (Pyle & Howell 2004, Powel 1987, Caldwell 1986, Erwin 1983, Rodgers
1980b, 1987, Werschkul 1979, Custer & Osborn 1978, Kushlan 1978a, Recher & Recher
1969). Quanto aos aspectos voltados ao estudo do seu comportamento podemos citar: i)
comportamentos alimentares, ou táticas de forrageio (Kelly et al. 2003, Rodgers 1983,
Willard 1977, Kushlan 1976a, 1978b); ii) comportamentos reprodutivos, ou posturas de
13
exibição sexuais (Werschkul 1982, Rodgers 1978, 1980a, Palmer 1962, Meyerriecks 1960,
Meanley 1955); iii) vocalizações e comunicação (Rodgers 1980a). Estudos com a espécie na
América do Sul são escassos, aparecendo a espécie juntamente com várias outras em um
estudo sobre cleptoparasitismo na Venezuela (González 1996); e mais especificamente como
sujeito do estudo em um trabalho sobre sua ecologia reprodutiva em Cubatão-Santos/SP
(Olmos & Silva e Silva 2002, Olmos et al. 2001), como o único feito com a espécie no Brasil.
Da mesma forma, as interações comportamentais de indivíduos durante o forrageio não foram
estudas de forma mais aprofundada para a espécie por nenhum autor.
14
Objetivos
1. Descrever a territorialidade alimentar da garça-azul, Egretta caerulea, em uma área
estuarina (manuscrito 1):
a. Averiguar a defesa de território para a espécie;
b. Caracterizar a distribuição e o uso de área para a alimentação;
c. Analisar as influências da defesa territorial sobre o investimento e o sucesso de
forrageio.
2. Descrever os comportamentos realizados pela espécie durante as interações sociais
durante o forrageio (manuscrito 2):
a. Descrever as posturas de exibição realizadas durante o período de forrageio;
b. Descrever as vocalizações realizadas durante o período de forrageio;
c. Descrever as interações entre indivíduos no período de forrageio.
3. Caracterizar os comportamentos associados à defesa territorial em Egretta caerulea
(manuscrito 3):
a. Verificar a freqüência de ocorrência dos comportamentos expressos pelos
indivíduos territoriais;
b. Determinar freqüência, duração e latência dos comportamentos expressos
durante a defesa territorial.
15
Manuscrito 1
Título – Territorialidade Alimentar na Garça-azul, Egretta caerulea, em Cananéia, Brasil.
Autores - Emmanuel Moralez-Silva
1
, Flávio José de Lima Silva
2
e Emygdio Leite de Araujo
Monteiro-Filho
3
.
1
– Pós-Graduação em Psicobiologia – Estudos do Comportamento, Universidade Federal do
Rio Grande do Norte, Brazil. Instituto de Pesquisas Cananéia (IPeC), 199 Tristão Lobo,
Centro, Cananéia, SP, 11.990-000, Brazil.
2
- Laboratório de sistemática e Ecologia Animal, Dept. de Ciências Biológicas, Universidade
do Estado do Rio Grande do Norte. Mossoró-RN.
3
- Departamento de Zoologia, Setor de Ciências Biológicas, Centro Politécnico, Universidade
Federal do Paraná, PO Box 19020, Curitiba, PR, 81.531-990, Brazil. Instituto de Pesquisas
Cananéia (IPeC), 199 Tristão Lobo, Centro, Cananéia, SP, 11.990-000, Brazil.
Periódico – Journal of Animal Ecology, QUALIS A.
Status – a ser submetido.
16
Resumo
1. O uso do habitat pela garça-azul, Egretta caerulea, e a descoberta da territorialidade
alimentar na mesma é apresentado neste trabalho.
2. Os resultados mostraram a existência de um indivíduo territorial defendendo uma área
(2564,46 ± 943,56m²) próxima ao manguezal; e indivíduos não-territoriais (9,17 ±
2,54) no restante da área demarcada (área: 893,25 ± 676,72).
3. Uma correlação positiva fraca (r=0,47, df=46, p<0,05) foi encontrada entre o número
de sobreposições entre o indivíduo territorial e os não-territoriais (2,85 ± 3,07) e a
média de área sobreposta para o indivíduo territorial (171,41 ± 131,40 m²).
4. Maiores taxas de captura (1,52 ± 1,14 x 1,00 ± 1,37 capturas/min) e sucesso (0,45 ±
0,31 x 0,21 ± 0,27), e menores taxas de gasto de energia (45,21 ± 14,96 x 51,22 ±
14,37 passos/min; e 3,65 ± 2,55 x 4,94 ± 3,28 tentativas de captura/min) foram
observadas para indivíduos forrageando em áreas mais próximas à margem.
5. Estes resultados sugerem que o comportamento territorial observado para a garça-azul
está mais relacionado a algum parâmetro alimentar do que à pressão de intrusos.
Ainda, que a territorialidade pode estar relacionada à defesa de áreas que apresentam
maior disponibilidade de presas.
17
Title Page
Title - Feeding Territoriality in the Little Blue Heron, Egretta caerulea, in Canaéia, Brazil.
Authors - Emmanuel Moralez-Silva
1
, Flávio José de Lima Silva
2
and Emygdio Leite de
Araujo Monteiro-Filho
3
.
1 – Pós-Graduação em Psicobiologia – Estudos do Comportamento, Universidade Federal do
Rio Grande do Norte, Brazil. Instituto de Pesquisas Cananéia (IPeC), 199 Tristão Lobo,
Centro, Cananéia, SP, 11.990-000, Brazil.
2 - Laboratório de sistemática e Ecologia Animal, Dept. de Ciências Biológicas, Universidade
do Estado do Rio Grande do Norte. Mossoró-RN.
3 - Departamento de Zoologia, Setor de Ciências Biológicas, Centro Politécnico,
Universidade Federal do Paraná, PO Box 19020, Curitiba, PR, 81.531-990, Brazil. Instituto
de Pesquisas Cananéia (IPeC).
Corresponding Author - Emmanuel Moralez-Silva, 3460 Alameda dos Bosques, Parque das
Nascentes, Pinhais, PR, 83.320-970, Brazil, [email protected].
Running headline - Territoriality in the Little Blue Heron.
18
Summary
1. The use of the habitat by the Little Blue Heron, Egretta caerulea (Linnaeus 1758), and
the discovery of the feeding territoriality for the specie is brought here.
2. The results showed the existence of a territorial individual defending in an area
(2564.46 ± 943.56m²) closest to the mangrove, and non-territorial individuals (9.17 ±
2.54) in the rest of a demarcated area (area: 893.25 ± 676.72).
3. A week positive correlation (r=0.47, df=46, p<0.05) was found between the number of
overlapping between the territorial individual and the non-territorial ones (2.85 ± 3.07)
and the mean of overlapped area for the territorial individual (171,41 ± 131,40 m²).
4. Higher capture (1.52 ± 1.14 x 1.00 ± 1.37 catches/min) and success rates (0.45 ± 0.31
x 0.21 ± 0.27) and lower energy expenditure rates (45.21 ± 14.96 x 51.22 ± 14.37
steps/min; and 3.65 ± 2.55 x 4.94 ± 3.28 stabs/min) were observed for individuals
foraging in areas closest to the mangrove.
5. Our results suggest that the territorial behavior observed has more relation to some
food parameters than to the intruder’s pressure, and also that the territoriality observed
might be related to the defense of areas with higher availability of prey.
Key words – Actuation area, Cananéia estuarine system, Defense, Mud bank, Territory.
19
Introduction
The Little Blue Heron, Egretta caerulea, is a specie that is found in all the American
continent, and that has a more coastal distribution in South America, and yet very related to
estuarine systems (Sick 1997). Its behavior and ecology have been well studied in other parts
of the continent (Recher & Recher 1969; Kushlan 1978a; Werschkul 1979,1982; Rodgers
1980a, b, 1987; Erwin 1983; Caldwell 1986; Pyle & Howell 2004; and others); but specific
studies of its foraging behavior, as to the dynamics and not the foraging strategies (Kushlan
1976, 1978b; Willard 1977; Rodgers 1983; Kelly, Gawlik & Kieekbusch 2003), have not yet
been very well accessed; and also, studies on this specie in the latest years are few, especially
in South America (Olmos, Silva e Silva & Prado 2001; Olmos & Silva e Silva 2002).
The use of the feeding site is related to its physical as well as to its biological features,
in which the characteristics of the prey are a very important factor (Kushlan 1981). According
to Kushlan (1981), ciconiiforms aggregate in an area of hight prey availability, are more or
less attracted by other birds, specially the white species (Kushlan 1977, 1979; Caldwell 1981;
Smith 1995), and have certain advantages for this. Thus, the relationships that an individual
has with others (Ricklefs 2001) are very important to the outcome of its behavioral success,
therefore its survival and reproduction acting on its fitness (Alcock 2005).
The defense of an important resource, been it the nest material, food supply, the mate
and so on, acts as an important factor in increasing the individuals chances of success.
According to Noble (1939), the defense of any area characterizes this as a territory; and
further more, we are in agreement to the definition that a territory is a fixed space from which
an individual or group of mutually tolerant individuals excludes competitors from a specific
resource or resources (Maher & Lott 1995). To demonstrate the existence of a territory in a
given specie, three factors must be simultaneously met (Brown & Orians 1970): a territory
must be (i) exclusive, (ii) fixed and (iii) actively or passively defended against intruders.
20
These three factors have been found in territorial behavior of various species of vertebrates,
and observed for different groups of birds (Maher and Lott 2000).
It is well known for colonially breeding birds, including the Ciconiiformes, the
defense of the surroundings of the nest (Nice 1941). And the observation of these territories
has been made for almost every species that has had its breeding biology studied. On the other
hand, the feeding territoriality of this group has not been much documented. Two of the few
species that have had its territorial behavior better studied are the Grey Heron, Ardea cinerea,
by Richner (1986) and Marion (1989), and the Little Egret, Egretta garzeta, by Yamada
(1994) and Nota (2003). Thus, in this study the aim was to describe the feeding territoriality
of the Little Blue Heron in an estuarine system in Brazil, investigating the territorial defense
for the specie; characterizing its distribution and use of feeding habitat, and analyzing the
influences of the territorial defense over the foraging investment and success.
Materials and methods
Study area - The study was conducted in the Complexo Estuarino Lagunar de Iguape-
Cananéia, which is a great estuarine-lagoon system, of approximately 110Km of extension, in
the south coast of São Paulo state in southeastern Brazil (from 25° 00` to 25° 04` S and 47°
54` to 47° 56` E). This system is formed by three islands: Ilha de Cananéia, Ilha Comprida
and Ilha do Cardoso, which forms channels and lagoons that are connected to the open sea
(Fig 1a).
The predominant vegetation in the channels is the mangroves, composed by three
main species: black mangrove, Avicennia schaueriana; red mangrove, Rhizophora mangle;
and white mangrove, Laguncularia racemosa (Schaeffer-Novelli, Mesquita & Conturón-
Molero 1990). The mud banks are very common on the channels margins, and are margined
by a few species of the Poaceae gender Spartina, which are adapted to live in estuarine
21
regions (Schaeffer-Novelli, Mesquita & Conturón-Molero 1990). These mud banks are under
the influence of the tidal cycles, been exposed by the low tide and covered by the hight tide.
A specific mud bank in the island Ilha de Cananéia, called Brocuanha mud bank, was
used for this study. It is located in the south portion of the island, close to the city, and it has
approximately 1500m of extension by 110m width (▲, in Fig 1a). This area is used as a
feeding site by different species of herons and egrets throughout the year.
Determination of the actuation areas - To determine the actuation area of different
individuals, an area of approximately 12600m² of the Brocuanha mud bank was demarcated
with 24 wood stacks – with dimensions of 1.50m or 2.50m of extension and 5cm of thickness
– painted with minium for durability. A small wood plaque – 15x10x4cm – also recovered
with minium and painted and numbered with oil ink was placed on the point of each stack.
The stacks were fixed on the mud bank, during the hight tide with the help of a bout,
in three lines parallel to the margin. To the first line, closest to the margin, 8 stacks of 1.50m
were used, and placed 30m away from each other. The other two lines were placed using 8
stacks of 2.50m for each one. The second line was 30m away from the first and the third also
30m away from the second, in the direction of the water channel. As in the first line, the
stacks were placed 30m away from each other, forming 14 quadrants of 30x30m each, in two
lines of seven quadrants, side by side (e.g., Fig. 1b). The observation point is in a pier already
existent, which was used as reference for measuring the distance of the first couple of stacks,
thus been located in the center of the demarcated area. By this quadrants distribution it is
possible to access the distribution of individuals inside a specific area of the feeding site.
22
Figure 1.a) Map of part of the Iguape-Cananéia estuarine lagoon system, southeastern Brazil,
sowing the Brocuanha mud bank (▲). b) Scheme of the demarcated area with the two lines of
seven quadrants (30x30m). The three sectors are represented by the areas between the
horizontal lines.
The procedures to determine the actuation areas of different individuals were as
follows. The observation was divided into 30min period sessions (chosen arbitrarily because it
was a period of time which allowed a significant quantity of data to the analysis, without
1 2
3
9 10
11
4 5 6
12
13
14
15
7 8
16
24 23 22 21 20 19 18 17
OBSERVATION
POINT
SECTOR 1
SECTOR 2
SECTOR 3
B
23
being overwhelming on the observer). In each session, the individuals using the demarcated
area (mean=9.17, Lower95%=8.45, Uper95%=9.89) to forage were accompanied,
simultaneously and by naked eyes (during the whole time the individual stayed inside the
area), and its trajectory would be continuously registered in a sheet with the quadrants
disposition. This is possible doe to the foraging method of the specie, that is by a continuously
slow walking (locomotion of ≤ 1 step/sec, cf. Rodgers 1983). By the beginning of the session,
each individual inside the demarcated area received an identification number, for its
identification on the work sheet, and its trajectories were registered until the end of the
session or until the individual leaved the demarcated area. When an individual would leave
the demarcated area, it would no longer be registered, and every time a new individual would
enter the demarcated area, it would begin to be registered. It is important to establish that the
individuals were not captured and marked artificially; they were only differentiated from each
other by the observer by its location in the demarcated area. Combining up the low number of
individuals simultaneously foraging inside the demarcated area (mean=9.17,
Lower95%=8.45, Uper95%=9.89) and the slow walking method of foraging by the specie, the
accompaniment of the individuals foraging simultaneously in the demarcated area and the
registration of their trajectories was possible. As the individuals were not marked, it could be
possible that one individual that eventually lived the demarcated area and returned yet in the
same session would be registered twice, and this probably has happened a few times during
the study.
The determination of the actuation area of the different individuals was made using the
minimum convex polygon method (MCP). The data from the polygons was than transferred to
the software AutoCAD LT 2004 for the determination of the sizes of the actuation areas of the
different individuals. With the sizes of the areas was possible to calculate both the sizes of the
overlapped areas between individuals and the overlapping percentage between them. For this
24
quantification were used only the data from the individuals that spend more than 66,66%, or
20min, of the session time (30min) foraging inside the demarcated area, to have a significant
quantity of data for each individual.
Determination of foraging parameters - According to Kushlan (1978a) the foraging effort,
and consequently the energy expenditure of foraging Little Blue Heron can be assessed by the
number of steps that an individual takes in one minute and also by the number of stabs that it
gives in one minute. And the foraging success of an individual can be assessed by the number
of catches in one minute and by the rate of catches per stabs. Following this method, we
collected data for all these parameters from the Little Blue Herons foraging in the Brocuanha
mud bank. These data were collected from individuals foraging in three different areas in the
mud bank. The first was the area between the first and second lines of stacks of the
demarcated area, and designated sector 1. The second was the area between the second and
third lines of stacks, been it the sector 2. And the area behind the third line of stacks
comprehended the sector 3 (e.g., Fig. 1b). The sectors 1 and 2 together comprehend about half
of the mud bank width, and the sector 3 about the other half.
Results
The study had a total of 120 hours, from May 2005 to February 2006. The number of
individuals decreased trough ought the study period (Fig 2).
25
m
j
j
a
s
o
n
d
j
f
0
50
100
150
200
250
Months of study
Mean number of individuals
Figure 2. Mean ± SD number of Little Blue Herons present in the mud bank area trough the
ten studied months.
Foraging Parameters - For all four foraging parameters it was performed the Kruskal-Wallis
one way ANOVA test to comparisons between the three sectors, with statistical significance
considered at α=0.05.
The individuals foraging in the sector 1 and 2 made less capture effort. The number of
steps per minute (sector 1 - 45.21 ± 14.96; sector 2 – 44.19 ± 13.63: n-number of observations
=335, H=18.20, P<0,05) and the number of stabs per minute (sector 1 – 3.65 ±2.55; sector 2 –
3.25 ± 2.93: n=335, H=21,19, P<0,05) for these individuals were significantly lower than for
those individuals foraging in the sector 3 (51.22 ± 14.37 steps/min; 4.94 ± 3.28 stabs/min)
(Figs. 3a, b). On the contrary, the individuals foraging in the sector 3 had less foraging
success. The number of catches per minute (n=318, H=21.95, P<0,05) and the rate of catches
per stabs (n=318, H=39.30, P<0,05) for individuals of the sector 3 (1.00 ± 1.37 catches/min;
0.21 ± 0.27 catches/stabs) were significantly lower than for those individuals foraging in
sectors 1 (1.52 ± 1.14 catches/min; 0.45 ± 0.31 catches/stabs) and 2 (1.45 ± 1.37 catches/min;
0.44 ± 0.36 catches/stabs) (Figs 3c, d).
26
A
1
2
3
0
20
40
60
80
100
Sectors
Number of steps / min
B
1 2 3
0
5
10
15
20
Sectors
Number of stabs / min
C
1
2
3
0
2
4
6
8
Sectors
Number of catches / min
D
1
2
3
0.0
0.5
1.0
1.5
Sectors
Number of catches / stabs
Figure 3.a) Number of steps from the individuals of Little Blue Heron foraging in the three
different sectors in the mud bank, in the Cananéia estuary. b) Number of stabs from the
individuals of Little Blue Heron foraging in the three different sectors in the mud bank. c)
Number of catches from the individuals of Little Blue Heron foraging in the three different
sectors in the mud bank. d) Success rate (catches/stabs) from the individuals foraging in the
three different sectors in the mud bank. Values are given as median, with the whiskers
representing minimum to maximum value.
Territoriality - Inside the demarcated area, one individual holding a feeding territory was
observed every day. This individual would arrive in the area in the beginning of the feeding
period, when the low tide had begun to expose the mud bank, and stayed defending a
27
particular area, never leaving this area, until the end of the feeding period, when the hight tide
had already covered the mud bank.
All the other individuals in the demarcated area would not exhibit this kind of
behavior, been non-territorial. These individuals would also arrive in the beginning of the
feeding period and stay until its end, but they would occupy the same areas, simultaneously
and not exhibiting a defense behavior. The territorial individual expelled any other individuals
that would enter on the patrolled area (Fig. 4c), being adults as well as immature ones. In the
Figures 4a and b there are the representation of two of the 30min observation periods, in with
are represented in black the territorial individual, and in grey the non-territorial individuals
that utilized the area in these observational sessions. The area defended by the territorial
individual was in the mud bank area closest to the mangrove, occupying the sector 1 and part
of the sector 2.
28
TERRITORIAL
NON-TERRITORIAL
Figure 4. a/b) The results of two 30min observation sessions taken to determine the actuation
areas of different Little Blue Heron individuals foraging in the demarcated area, in the
Cananéia estuary. c) Representation of the entire area occupied by the territorial individual
trough the study period and the area of most exclusive use.
In table 1 are presented the results for the sizes of the actuation areas of the territorial
and non-territorial individuals, as well as the sizes and percentages of the overlapped areas
between the territorial individual and the non-territorial, and between the non-territorial
individuals themselves. It was chosen to perform the non-parametric Wilcoxon test, because
B
C
29
the variances between the two groups were considered too different (Bartlett test F=176.47,
P<0.05) and the N of the groups were also very different. It can be observed that the total
area for the territorial individual is bigger than that of the non-territorial ones (n=1096, Z=-
10.01, P<0.05), and that the overlapping percentage of area is small for the territorial
individual than for the non-territorial ones.
The total area patrolled by the territorial individual was of approximately 8800.56m².
The defended area, the one it was successful in keeping others entirely out was of about
1849.64m². The area patrolled by the territorial individual corresponds to approximately
5.87% of the mud bank area (approximately 150000m²) (see Fig 4c). If we consider the
average number of individuals feeding in the mud bank (137 individuals) from May to August
(the months that had more individuals), than the area per individual, out the 1849.64m² of the
territorial one, is about 1081.39m².
Pearson’s correlation was performed (n=120, r=0.03, df= 46, P>0.05) between the
average number of individuals in the demarcated area (mean=9.17, lower95%=8.45,
uper95%=9.89) and the average of overlapped area for the territorial individual (Table 1), and
the average number of overlapping between the territorial individual and the non-territorial
ones (mean=2.85, lower95%=2.33, uper95%=3.38) (n=120, r=0.14, df=46, P>0.05). A week
correlation between the number of overlapping between the territorial individual and the non-
territorial ones and the average of overlapped area for the territorial individual was observed
(n=120,r=0.47,df=46,P<0.05).
In 100% of the days from May to August, a territorial individual was present in the
mud bank, always defending the same area (Figs. 4a,b,c). But from September to December a
territorial individual was absent, that is, no defense was observed.
30
Table 1. Values on the sizes of actuation areas for the territorial and non-territorial individuals (average total area); average overlapped
area between the non-territorial individuals and the territorial, and between the non-territorial among each other; and the overlapping
percentage for the territorial and non-territorial individuals. For the feeding Little Blue Heron in Cananéia, southeastern Brazil. The n
values regard the 30 min period sessions of data collection.
n
average
total area
(m²) SD
lower
95%
uper
95%
average
overlapped
area ( m²) SD
lower
95%
uper
95%
overlapping
percentage
(%) SD
lower
95%
uper
95%
territorial 120
2564.46 943.56
2375.71 2753.21
171.41*
131.40
144.78 198.03 8.48 5.90 7.30 9.66
non-territorial 976
893.25 676.72
830.99 957.51
633.98
560.67
580.58 687.37 66.80 22.71
64.65
68.96
* The boldface values regard the average of the data statistically tested with the Wilcoxon-test.
31
Discussion
It is know for the populations of Little Blue Heron of the North hemisphere that
migration occurs from feeding sites to colony sites, and the other way around (Dusi 1967).
Richner (1986) observed the abandonment of feeding territories at the start of the breeding
season for the Grey Heron. Therefore, the decreasing in the number of individuals, especially
from August might be related to a migration to the reproductive areas. This specie is yet
starting to be better studied in Brazil, and the colony sites and the dislocation of individuals
from different areas as to feeding sites or colony sites, it is not know. But this hypothesis
seems to be very plausible, because as the observed in the results of the present study, there is
a possible abandonment of a territorial individual from the area in the reproductive months
(September to December) and a possible return in the end of the reproductive period
(January). The territorial individual was always an adult, and so, probably a reproductive one.
The colony sites are not know yet, but from our observations of the decreasing in the
number of individuals and the absence of a territorial individual in the reproductive months, it
can be argued that probably the colony sites are too distant from the Brocuanha mud bank;
since it is accepted that the proximity to the feeding areas is an important factor for the
selection of breeding sites in herons and egrets (Gibbs et al. 1987). According to Custer and
Osborn (1978), herons must feed within a certain range of the colony; a distance at which it is
energetically feasible for they to fly between foraging areas and the colony. Then, since there
is an abandonment of the area during the reproductive period, it is possible that the new
feeding area is close to the colony.
Territoriality is difficult to prove because of the tenuous difference between
aggressive behavior of a territorial individual and the defense of individual distances among
individuals (Marion 1989). To demonstrate the territoriality in herons one needs to follow
identifiable individuals over a significant period with a marking system that can be located
from distance (Marion 1989). However, with the method used here, we were able to
32
demonstrate the territoriality of the Little Blue Heron without having to mark individual birds,
and from a very close distance of the feeding site and the birds. This is probably because the
behavior of the species in the area is very docile in the sense of permitting the presence of the
observer, and also because of the very fixed way of using the feeding site by the territorial
individual.
The method of stakes can give us a size of the territory very close to the real, since the
points used to create the polygon are taken from the observation of the trajectory of one
individual been accompanied by the observer eyes at a whole period of time. Different from
the territory and home range sizes established from spot observations of the male or the
reproductive pair of a bird species or the various capture points of a mammal (Odum &
Kuenzler 1955).
Our observations here lead to define the territorial individual as such for its behavior is
attending the three simultaneous conditions proposed by Brown and Orians (1970) as
necessary to be met when attempting to show territoriality. The first says that a territory must
show a slow change over time, or be fixed; what was very clear for the Little Blue Heron in
here. The second is about exclusivity and that was another condition verified here. And the
third condition, which was also observed in our study, is the active or passive defense of the
area against rivals.
Since the territorial behavior of the Little Blue Heron was observed out of the
reproductive station, corresponding to the winter, it can be suggested that this territory is a
kind of winter territory (or type E), and it is used in the feeding ground (Nice 1941; Wilson
1975).
The concept of economic defendability proposed by Brown (1964) and its outcome on
the evolution and adaptive significance of territoriality is a more accepted solution in
explaining the diversity of territorial systems in different species (as discussed by Verner
1977). In the lights of Darwin’s natural selection theory, this concept brings the relevance of
33
the individual’s behavior in enhancing its survival and reproduction, as well as its
contribution to the next generation’s gene pool, or its inclusive fitness (Alcock 2005). As said
by Davis and Houston (1984), “the concept of economic defendability states that we would
only expect an animal to spend time and energy interacting with others to defend a territory
when this yields greater net benefits than an alternative behavior, for example ignoring others
in the population and spending the whole time exploiting the resource”. If, aside the defended
area (restrict use) of the territorial individual, the other individuals feeding in the mud bank
have been left with approximately 1081.39m² of area per individual foraging; and if, as
observed by us, more territorial individuals would exist in the mud bank, then these areas
could be even smaller and almost totally overlapped (increase of overlapping in the use of
resources among individuals). Thus, the territorial behavior of a territorial individual could
actually be paying off, since it defends an area of exclusive use bigger than the area available
for each non-territorial individual, and in an area within the mud bank that could have more
prey available (see discussion below).
Since we are yet in the beginning of the studies on the territorial behavior of the Little
Blue Heron, it is a presumption to think that we would have answers regarding a more general
and wide-ranging solution in trying to explain the adaptiveness or evolution of this system.
But we can try to begin to understand a few reasons that might lead an individual Little Blue
Heron to defend a particular area in a mud bank, in a very productive estuary. Since we are
looking at a feeding territory, what it is been defended here is the food resource, and the
access to it. According to Brown and Orians (1970) it is generally assumed that food is the
defended resource when territories are established away from the breeding area. Davis and
Houston (1984) point that one of three factors favoring territoriality is the resource quality
and distribution. One of many reasons that can derive an animal to defend a certain portion of
a feeding site is the hight availability of prey at this area, what can bring it more prey with
less energy expenditure (Davis 1978). Varoli and Souza (1990) in a study of the benthonic
34
macro fauna in a series of mud banks in the Iguape-Cananéia estuarine-lagoon system found
that the areas closest to the margin (or the mangroves) have greater numbers of polychaetes,
mollusks, isopods, decapods, among others. These organisms form a rich prey source for
herons and other bird species. Our data on the foraging parameters shows that the area
comprehending the sectors 1 and 2, what correspond to approximately half of the mud bank
width, brings to the individuals foraging inside it greater gains with less energy expenditure
than the individuals foraging in the other half, comprehending the sector 3. The area of the
territorial individual extends from the sector 1 to a part of the sector 2, what comprehends
exactly the area pointed for Varoli and Souza (1990) as the area with more availability of prey
in the mud banks. This suggests that territorial birds defend patches of abundant food
resources which might confer unique energetic benefits to the territorial individual, as
observed by Turpie (1995) and Tripp and Collazo (1997). This can be one of many possible
explanations to account the reasons for why an individual defends an area in the Brocuanha
mud bank, as observed by us and exhibited in here.
The correlations don’t denote a cause and effect relationship, but they can be used to
some considerations. It is intuitive to think that there would be some relation between the
number of individuals and the number of overlaps between the territorial and non-territorial
individuals, and the mean size of the overlapping between them. As to think that much more
individuals present in the area, an increase of the density of individuals (potential
competitors) would increase these relations, as observed by some researchers in studies of
intruder’s pressure on territory size (Myers, Connors & Pitelka 1979; Ewald, Hunt & Warner
1980; Norton, Arcese & Ewald 1982; Dunk & Cooper 1994; Tripp & Collazo 1997; Wronski
& Plath 2006). But it seams that maybe this is not the case here for the Little Blue Heron.
Following this line of thought, on the other hand, the positive correlation found between the
number of overlapping and the mean size of the overlapped area for the territorial individual
might be cautiously interpreted as mining that a possible increase in the number of individuals
35
in the area might increase the size of the total area that the intruders might occupy inside the
territorial individuals area. These results might suggest that the intruder density does not have
such an important role in the territorial behavior of the Little Blue Heron; and that some
characteristics of the preys play a more expressive role (see discussion on this subject in
Myers, Connors & Pitelka 1979; Hixon 1980; Tripp & Collazo 1997).
The territoriality in colonial birds is wide accepted (Nice 1941), principally
concerning the reproductive period, considering the area surrounding the nest the territory.
But true feeding territories have been prove to exist for the Little Egret (Yamada 1994; Nota
2003), the Grey Heron (Richner 1986; Marion 1989), the Reef Heron (Recher 1972), as we
also found for the Little Blue Heron. Hancock and Kushlan (1984) affirm that the Goliath
Heron, Ardea goliath, the Black Heron, Egretta ardesiaca, the Tricolored Heron, Egretta
tricolor, and the Black-crowned Night Heron, Nycticorax nycticorax, also exhibits feeding
territoriality. And Lowe (1983) observed also the White-faced Heron, Egretta
novaehollandiae, defending feeding territories in mudflat areas. But actual data confirming
these observations is unclear. Yet, Kushlan et al. (1982) suggests possible holding of feeding
territories by Whistling Herons, Sirigma sibilatrix. For the Little Blue Heron, Palmer (1962)
wrote that individuals vigorously defend feeding territories out of the reproductive period. As
in the cases above, this is yet too little information to affirm the true existence of feeding
territories for the species. But with the results in here, this existence became real.
Our results show that in one day of observation, the individual defending the territory
in the mud bank is always the same, since it arrived at the beginning of the feeding period and
stayed until its end. Future studies should consider marking individual birds that frequent the
feeding site to access the possible fidelity of area throughout an entire season.
36
Acknowledgments
We thank the Instituto de Pesquisas Cananéia (IPeC) for all the support, with material, field
assistance and logistic. And we also thank the engineer Thelicia Silva for the support with the
AutoCAD LT 2004 software. Finantial support, in form of a scholarship, is acknowledged
from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).
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40
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41
O autor Emygdio L. A. Monteiro-Filho colaborou desde o início do trabalho, no ano de 2005.
Ajudando com a elaboração do projeto, assim como da dissertação e dos manuscritos,
contribuindo para a discussão dos resultados encontrados e suas relações com espectos
comportamentais e ecológicos. Esteve sempre presente, disponibilizando na forma de sua
pessoa ou do Instituto de Pesquisas Cananéia (IPeC), material bibliográfico e ajuda com a
logistica do trabalho de campo.
Journal of Animal Ecology – Formatação.
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43
Holyoak, M. (1993) New insights into testing for density dependence. Oecologia, 93, 435-
440.
Warham, J. (1996) The Behaviour, Population Biology and Physiology of the Petrels.
Academic Press, London.
Møller, A.P. (1997) Parasitism and the evolution of host life history. Host-Parasite Evolution
(eds D.H. Clayton & J. Moore), pp. 105-127. Oxford University Press, Oxford.
Stevenson, I.R. (1994) Male-biased mortality in Soay sheep. PhD thesis, University of
Cambridge, Cambridge.
44
Manuscrito 2
Título – Comportamento Social da Garça–azul, ao Forrageio, no Sudeste do Brasil.
Autores - Emmanuel Moralez-Silva
1
, Flávio José de Lima Silva
2
and Emygdio Leite de
Araujo Monteiro-Filho
3
.
1
– Pós-Graduação em Psicobiologia – Estudos do Comportamento, Universidade Federal do
Rio Grande do Norte, Brazil. Instituto de Pesquisas Cananéia (IPeC), 199 Tristão Lobo,
Centro, Cananéia, SP, 11.990-000, Brazil.
2
- Laboratório de sistemática e Ecologia Animal, Dept. de Ciências Biológicas, Universidade
do Estado do Rio Grande do Norte. Mossoró-RN.
3
- Departamento de Zoologia, Setor de Ciências Biológicas, Centro Politécnico, Universidade
Federal do Paraná, PO Box 19020, Curitiba, PR, 81.531-990, Brazil. Instituto de Pesquisas
Cananéia (IPeC), 199 Tristão Lobo, Centro, Cananéia, SP, 11.990-000, Brazil.
Periódico – Journal of Ethology, QUALIS A.
Status – a ser submetido.
45
Resumo
O comportamento social da garça-azul, Egretta caerulea, tem sido estudado somente no
período reprodutivo (posturas e comportamentos associados à reprodução). Os
comportamentos/posturas associados às interações de garças forrageando nas áreas de
alimentação ainda não foram estudados mais detalhadamente. Desta forma, o objetivo deste
estudo é apresentar uma análise descritiva das interações entre conspecíficos alimentando-se
em agregação, em um baixio lodoso, no sudeste do Brasil. Os métodos ad libitum e
amostragem comportamental foram utilizados para a descrição dos comportamentos. Quatro
tipos de posturas foram identificados; duas previamente descritos (Asas-espalhadas –
“Spread-wings” e Agachada – “Withdraw Crouch”) e duas novas (Estendida – “Extended” e
Asas alinhadas – “Wings Lined-up”). Uma vocalização, o chamado Ahh-ahh-ahh; e quatro
tipos de interações entre dois ou mais indivíduos, envolvendo ou não as posturas: i) Encontro;
ii) Briga; iii) Expulsão, e iv) Cleptoparasitismo. Todos estes comportamentos estão
relacionados, direta ou indiretamente, à dominância de uma área em particular, por um
indivíduo, contendo recurso alimentar. Isto aponta para a importância das interações sociais
entre garças forrageando, enquanto alimentam-se em grandes números em agregações
situadas em áreas ecologicamente importantes.
46
Title - Social Behavior of Foraging Little Blue Heron in Southeastern Brazil.
Emmanuel Moralez-Silva
1
, Flávio José de Lima Silva
2
and Emygdio Leite de Araujo
Monteiro-Filho
3
.
1
– Programa de Pós-graduação em Psicobiologia – Estudos do Comportamento, Universidade
Federal do Rio Grande do Norte (UFRN), PO Box 1511, Natal, RN, 59078-970, Brazil.
Instituto de Pesquisas Cananéia (IPeC), 199 Tristão Lobo, Centro, Cananéia, SP, 11.990-000,
Brazil.
2
– Programa de Pós-graduação em Psicobiologia – Estudos do Comportamento, Universidade
Federal do Rio Grande do Norte (UFRN).
Laboratório de sistemática e Ecologia Animal, Dept. de Ciências Biológicas, Universidade do
Estado do Rio Grande do Norte, Mossoró, RN, Brazil.
3
– Departamento de Zoologia, Setor de Ciências Biológicas, Centro Politécnico,
Universidade Federal do Paraná, PO Box 19020, Curitiba, PR, 81.531-990, Brazil. Instituto
de Pesquisas Cananéia (IPeC).
Total text pages: 24
Number of tables and figures: 5
Send proofs to: Emmanuel Moralez-Silva – 3460 Alameda dos Bosques, Parque das
Nascentes, Pinhais, PR, 83.320-970, Brazil, m[email protected]. Telephone: 55 41
3669 7506, fax: 55 41 3668 3412.
47
Abstract
The social behavior of the Little Blue Heron, Egretta caerulea, has been studied only during
the breeding period (displays associated to the breeding behavior). The displays associated to
the interactions of foraging herons in the feeding grounds have not yet been studied more
detailed. Therefore, the aim of this study is to present a descriptive analysis of the interactions
between conspecifics feeding in an aggregation, in a mud bank, in southeast Brazil. The
methods of ad libitum and behavioral sampling were used to describe the behaviors. Four
types of display postures were identified, two previously described in the literature (Spread-
wings and Withdraw Crouch) and two new ones (Extended and Wings Lined-up). One
vocalization, the Ahh-ahh-ahh call. And four types of interactions between two or more
individuals, involving or not the display postures: i) Encounter; ii) Fight; iii) Expulsion, and
iv) Kleptoparasitism. All these behaviors are related, direct or indirectly, to the dominance of
a particular area of food resource by one individual. And then, pointing out to the importance
of the social interactions between foraging herons, as they feed in great numbers on
aggregations in ecologically important areas.
Key words: Cananéia estuarine system, Display postures, Dispute, Description, Herons,
Interactions.
48
Introduction
The term social can have several connotations, and different researchers use it in slightly
different manners. For ones, this term is used in a restrict sense, to animals that exhibit a
certain amount of familial dependence, those bearing elaborate behavioral displays, or those
living within demographically structured groups (Giraldeau and Caraco 2000). Others use the
term more widely, and consider being social any animal that spends a good part of its life in
groups that are open, unstructured and temporary (Giraldeau and Caraco 2000).
This discussion was most vigorous with the flowering of the classic Ethology, and
ethologists as Lorenz and Tinbergen tended to distinguish really social groups from
aggregations (gatherings of nonsocial animals). These aggregations would form accidentally;
while true social groups would form as a result of a genuine attraction between individuals
(Giraldeau and Caraco 2000).
Latter in the twenty century, the incorporation of the evolutionary perspective in the
study of the behavior, and the emerging of the Behavioral Ecology, bringing a more
ecological-evolutionary approach, this form of using the term social became more bonded to
the functional level (Krebs and Davis 1993). This evolutionary perspective of social groups is
more concerned that individuals in a group are interdependent and their actions has
consequences on their fitness gains and pay offs, operating on the costs and benefits of their
choices (Krebs and Davis 1991).
Therefore, and take to account that herons are known to form feeding aggregations at
proper sites (Kushlan 1981), these interactions can be considered as having a strong social
component. Various studies on the social feeding by herons and egrets had been done;
referring to its formation, structure and dynamics (Smith 1995, Master 1992, Erwin 1983,
1984, Kushlan et al. 1985, Kushlan 1976b, 1977).
Behavioral studies based on description are more numerous on the sexual repertory of
the social behavior of the species (Great Blue Heron, Ardea horodias – Mock 1976; Great
49
Egret, Ardea alba – Weise 1976 and Mock 1978; Black-crowned Night Heron, Nycticorax
nycticorax – Noble et al. 1938 and Palmer 1962; Yellow-crowned Night Heron, Nyctanassa
violocea – Bagley and Grau 1979; Snowy Egret, Egretta thula – Meyerriecks 1960 and
Palmer 1962; Reddish Egret, Egretta rufescens - Meyerriecks 1960; Tricolored Heron,
Egretta tricolor – Rodgers 1977, 1978b; Cattle Egret, Bubulcus ibis – Blaker 1969 and
Lancaster 1970; and Green Heron, Butorides virescens - Meyerriecks 1960).
The behaviors related to the foraging activities are well described (Kushlan 1976a, 1978a)
and studied (Papakostas et al. 2005, Battley et al. 2003, Richardson et al. 2001, Powel 1987,
Rodgers 1983, Hafner et al. 1982, Willard 1977). Yet, the behavioral interactions of foraging
herons at the intra-specific level are not much studied, although some workers do consider it
in their work (Blaker 1969, Pratt 1980, Garrido et al. 2002, Lekuona 2002, González 1996,
Wiggins 1991, Kushlan 1978b, 1981, Krebs 1974, Custer and Osborn 1978). Only Bayer
(1984a, b) have focused a study on the foraging ground displays and associated vocalizations
with the Great Blue Heron.
For the Little Blue Heron, Egretta caerulea, the sexual behavior and the related vocal
array were well studied by Rodgers (1978a, 1980), and also by Meanley (1955), Meyerriecks
(1960), Palmer (1962) and Werschkul (1982). The species has also had the foraging behavior
well studied, as cited above for the other species; but the behavioral interactions of
conspecifics at feeding grounds have not been studied more detailed.
The goal of this study was to describe the behaviors performed by the Little Blue
Heron during social interactions in the foraging period: i) describe the display postures held
during the feeding period; ii) describe the vocalizations performed during the feeding period;
and iii) describe the interactions between individuals during this period.
50
Study area
The study was made from May 2005 to February 2006, in a mud bank in the Cananéia-Iguape
estuarine lagoon system, in the south coast of São Paulo state, southeastern Brazil (from 25°
00` to 25° 04` S and 47° 54` to 47° 56` E). The system is composed by three islands, forming
a series of channels and lagoons, connected to the open sea; been then under the influence of
the daily tidal cycles. The mangroves are the predominant vegetation in the system, and in the
margins of the channels a series of mud banks are exposed by the low tides, serving as
feeding sites for the avifauna (more detailed description and map in Moralez-Silva et al.
manuscrito 1). Aggregations of foraging Little Blue Heron are common in these sites, varying
from approximately 20 to 200 individuals throughout the year (Moralez-Silva et al.
manuscrito 1).
Methods
The methods of ad libitum and behavioral sampling (Martin and Bateson 1993, Altmann
1974) were used to describe the behaviors here presented. The observations were made in a
fixed point (an existent pier), during the day, in the full or new moon and in the hours of low
tide, by naked eye or using a 10x50 binoculars. During the observational period, every time
two or more individuals were engaged in any sort of interaction, these would become center
of the attention, and its behaviors were registered. The description was a mist of the empirical
and functional method (cf. Lehner 1998); and also in terms of the individuals spatial relation
to features of the environment or to other individuals (Martin and Bateson 1993). The
observed behaviors were photographed and video recorded when possible as well.
The recording of the vocalizations were made from the same point of the behavioral
data collection. The sounds were recorded using an analog cassette tape recorder (Panasonic
Mini Cassette Recorder RQ-L31) connected to a Sennheiser directional microphone at a speed
of 19 cm/s. The recorded sounds were reproduced for analysis using the Raven Pro 1.2.1
software (Cornell Lab of Ornithology), and the physical parameters were obtained.
51
The recorded vocalizations were transferred to the Raven software and transformed in
spectrograms. From these spectrograms the physical parameters were obtained: frequency,
time of duration (both from the entire call, and the notes and intervals between notes) and
number of notes and visible harmonics. Frequency modulation, intensity and the distribution
of the energy in the vocalization could also be obtained.
Results
There were a total of 150 hours of behavioral observations during the nine months of
study.
Four types of display postures and four types of interactions between two or more
individuals were identified, involving or not the display postures.
Display postures
Extended (n – number of observations of such behavior=63) – the individual keeps the body
erect, almost on the vertical, with the head and neck extended and the head in line with the
neck, slightly up, with the bill closed. The wings are held very close to the body. No feather
erection is observed (Fig. 1).
Figure 1. Extended posture of Little Blue Heron in the Cananéia estuary feeding site.
52
Wings-lined-up (n=31) – the individual keeps the body horizontally to the ground, the neck
stretched and the head up, with the bill pointing upwards. One of the wings is lowered (the
one closest to the other individual), not passing the tarsometatarsus, and the other is pulled up
the back line. The rectrices are spread out on a medial length. No erection of the feather is
observed (Fig. 2).
Figure 2. Wings-lined-up posture of Little Blue Heron in the Cananéia estuary feeding site.
Spread-wings (cf. Bayer 1984b) - The heron maintain the body in a position as in the
Extended posture, and keeps the wings outstretched from the body. No dragging of the
substrate during the motion of the display was observed. This display was observed a few
times, and in all of them, the individual displaying it was fleeing from another.
We distinguished these last two displays because they happened in distinct contexts. The
Wings-lined-up was observed preceding a fight, and the Spread-wings, in the few times
observed, was performed by a heron fleeing from a conflict. It was never observed a transition
from one to the other, both happening separately and in distinct interactions.
Withdraw Crouch (n=55) (cf. Meyerriecks 1960) - the individual keeps the body in a more
low profile, horizontally to the ground, and maintain the neck also curved with the head
53
parallel to the ground. The wings are slightly drooped, but not passing the tarsal length. By
this, part of the back is exposed. Feather erection dos not occur.
All postures are used in the context of interaction with other individual; not used
alone. In all of these postures, no vocalizations were associated, and these could not be missed
since the observer was generally closer then 30 m from the displaying herons.
Vocalizations
Calls of low frequency and variable in intensity were recorded. These calls, named Ahh-ahh-
ahh call, can contain three to 10 notes of similar duration and with distinct frequency
modulation, spaced by each other in a low variable interval duration (Table 1, Fig. 3). The
energy is concentrated in the first harmonics, and not in the fundamental note. These results
were gathered by analyzing 25 recorded vocalizations from different individuals.
It is used primarily by territorial herons, but can also be used by non-territorial ones. It
can be observed that approximately only 10 to 15% of the individuals foraging in the mud
bank utilize this vocalization. Two instances of its use were identified, after an Expulsion and
after a short flight within the foraging area of the individual.
Figure 3. Spectrogram of Ahh-ahh-ahh call of Little Blue heron, Egretta caerulea, recorded
along interactions in a mud bank in Cananéia estuarine system, southeastern Brazil.
54
Table 1. Ahh-ahh-ahh call emitted by the Little Blue Heron, Egretta caerulea, during social
foraging in the Cananéia estuary, southeastern Brazil, with numbers of notes and physical
parameters (frequency (Hz), time (s), and numbers of visible harmonics). Values are given as
the mean ± SE.
Frequency range
(Hz)
Average
visible
harmonics
Average
notes
Average
duration of the
call (s)
Average
notes (s)
Average intervals
between notes (s)
693.02±164.98
1243.76±331.19
4.88±2.26 4.83±1.83
2.90±1.56
0.36±
0.14
0.26±0.08
Interactions between individuals
Encounter (n=57) – observed between two individuals, during approximately 1 to 2 min. They
came in to close proximity, approximately 2 to 3m of each other, and then assume the display
posture; or one of them can assume the Extended posture and the other the Withdraw Crouch
posture in the beginning of the interaction. Another case is when both of the individuals
assume the Extended posture, but if the encounter continues, one of them changes to the
Withdraw Crouch posture and moves further away from the other (Fig. 4). The encounter
terminates when the individual that had the Withdraw Crouch posture gets away from the
other one, by walking or flying. After this, both individuals then reassume foraging.
55
Figure 4. Encounter between two Little Blue Heron in the Cananéia estuary feeding site. The
individual in the right is assuming the Extended posture, and the individual in the left is
assuming the Withdrawn Crouch posture.
Fight (n=13) - Fights between individuals are the most rare interaction. They can evolve from
an Encounter or begin directly as the individuals met each other. Both individuals assume the
Wings Lined-up posture, with the wing down side turned to the opponent, and then walk in
circle turned one to the other. They start to jump towards each other, with the legs stretched
and beating the wings. Both individuals try to hit the other with the feet and peck on each
other, reminding the fight behavior of domestic rosters. The fight finishes with the loser
running away, and the winner might promote a little chase.
Expulsion (n=132) – The expulsion occurs when an individual expel another individual from
an area, generally a territorial one expel an intruder. The defensive individual leaves the place
were it was foraging, flying, walking quickly or running, in direction of the intruder, and can
give an Ahh-ahh-ahh call as it lands. The intruder fly as it detects the approach of the
defensive one. The flight of the territorial individual is in a maximum height of 1m of the
ground, and it can maintain the neck curved or extended. When the defensive individual
56
chases the intruder by the ground, it normally beat the wings as it runs. Normally the bird
expels one individual at a time, but a few observations of it expelling two individuals at a time
were made too. During the flight, the heron dislocates with a more “patterned” wing beats.
Kleptoparasitism (n=42) – The stealing behavior was observed when an individual captured a
prey with more than 7cm, such as a crab (Callinectes sp.) or a fish (Synbranchus sp.), that
demands more handling time, and another one would came flying in its direction and attempt
to steal the captured prey. This behavior has a success of approximately 25%; in 11 of the 42
observations the individual managed to steal the prey.
Discussion
Two display postures, the Extended and the Wings-lined-up, are new both for the Little Blue
Heron behavior, as for the literature. For both, similar postures, from breeding and foraging
herons, as to the position of the body parts have been described (eg. Stretch, Alert, Upright
and Spread-wings – Bayer 1984b, Mock 1976, Meyerriecks 1960). The other two postures,
the Withdraw Crouch and the Spread-wings, were already described in the literature (Bayer
1984b, Meyerriecks 1960), and have been observed in foraging herons also by Bayer (1984b).
Although any definition will be somewhat controversial, it can be said that communication
occurs when a signal that evolve for the role is sent to a receiver and the recipient responds
(Goodenough et al. 1993). The displays observed in the Ardeidea are considered to have
evolved as part of the communicative repertory of the individuals, acting on the visual
channel of communication between them (Mock 1976). Since all the display postures we
identified here are used in agonistic interactions, they have probably evolved in a way that the
message to be passed on is linked to the establishment of individual relationships between the
individual birds. In a dyad, one of the individuals always leaves as the “winner”; then it can
be considered as the dominant individual in the interaction, having privilege accesses to the
resource disputed. Once dominance is attained, it is often flaunted with a badge or a
57
characteristic stature (Martín et al. 2007, Bókony et al. 2006, Osborne 2005, Goodenough et
al. 1993). In here, the displays would be used in this manner, as the initial stage in the
agonistic escalate.
Since the breeding behavior of the Little Blue Heron has not yet been studied in
Brazil, the displays associated to the pair formation and to the breeding cycle are not known.
Then, it is not possible to do a comparison of the displays and interactions between the
foraging and nesting periods (as did Bayer 1984b) of the populations that use the estuarine
areas in the coast. But if we compare it with the nesting behavior described by Rodgers
(1980) for the species in North America, only the Withdraw Crouch can be considered as
corresponding to the nesting displays. We do have similarities, but it seams that the behaviors
performed at feeding sites are distinct from the ones performed during the nesting period.
A complex of displays that have an extended neck position, with the bill held above
the horizontal (Vertical, Bittern Stance, Upright, Spread-wings, Vocal Rise and Stretch), is
suggested by Bayer (1984b). The Extended and the Wings-lined-up displays could then be
included in this complex. It could be possible that all these displays have the same
evolutionary origin, been specialized during the evolutionary process to different
environments and contexts. As suggested by Bayer (1984b), the Vertical and Bittern Stance
are related to signaling potential predators. The Strectch and Spread-wings serves as
appeasement and/or threat towards another individual during an agonistic encounter (Mock
1976, Bayer 1984b). But they are used in different contexts, the first occurring in nesting
areas and the second in foraging areas (Bayer 1984b). It is possible that the Extended and the
Wings Lined-up displays, both appearing to signal appeasement and/or threat, occurs for the
Little Blue Heron in the foraging areas, as the Spread-wings for the Great Blue Heron.
The erection of the feathers happens in the agonistic displays of the breeding period
(Upright, Forward, Twig Shake, and others) in all heron species studied (Palmer 1962, Mock
1976, 1978, Weise 1976, Rodgers 1977, 1980), and also in the displays common to both
58
nesting and foraging areas for the Great Blue Heron (Bayer 1984b). We did not observe it in
the displays of the Little Blue Heron in here. Bayer (1984b) also did not observed erection of
feathers for the Spread-wings, exclusive foraging ground display of the Great Blue Heron.
Since the foraging ground displays we identified for the Little Blue Heron seem to be distinct
from the nesting ones, the displays exclusive of foraging activities might have lost this
morphological characteristic during the evolutionary process.
Different from Bayer (1984a) that registered seven vocalizations (although part of
them is corresponding to the ones used during the reproductive behavior) for foraging Great
Blue Heron, we observed and registered only one vocalization for the foraging Little Blue
Heron. Its characteristics, frequency and duration of notes and intervals between notes, are
similar to the vocalizations of the Great Blue Heron (Bayer 1984b). The restrict use of the
Ahh-ahh-ahh call suggest that it might be an important component of the social organization
of the species during the foraging period. The low frequency of the sound is another
characteristic of this call that can be related to its social use; since by it’s been of low
frequency, it can be dissipated for long distances, reaching the goal of transmitting the
massage it contains.
Bayer (1984d) has described a very similar vocalization, the Roh-roh-roh call, of
similar frequency range, number and duration of notes, and duration of the intervals between
the notes (of low variance). The Roh-roh-roh call is yet used more by territorial, than by non-
territorial herons, and is also given spontaneously by territorial herons. These characteristics
suggests that the Roh-roh-roh call and the Ahh-ahh-ahh call might be a similar, or even
practically a same call, with intrinsic specific differences, but that has evolved together with
the feeding territorial behavior of non-breeding herons.
According to Mock (1976), the communication of herons can happen both by visual
and acoustic channels, and in an open environment the visual modality surpasses the acoustic.
But, as pointed by Mock, the visual signals can only reach the intended receiver if that
59
individual is oriented toward the sender. So the acoustic signals are used to maintain an open
visual channel (Mock 1976). All the displays we identified for the Little Blue Heron would
happen during an interaction with another individual (reactive displays, cf. Mock 1978); they
would never be performed by an individual that was alone, with no other in its surroundings.
This might explain the poor vocal array found, since it was not necessary for an individual to
drawn attention to it self by vocalizing, when the need of a display would appear only when
another individual would approach. This reinforces the possible function of the Ahh-ahh-ahh
call as a vocalization used in the social context of foraging, been related only to the Expulsion
interaction and not to any of the display postures.
Meyerriecks (1960) believes that the amount of neck extension reflects the degree of
escape tendencies. This might not be the case here, since as in the Encounter, the heron does
not show escape tendencies when performing the Extended posture, but does so when
performing the Withdrawn Crouch. Thus, in the social context of foraging in the Little Blue
Heron, the degree of extension of the neck might not be related to escape tendencies, been
more related to an attempt to appear bigger to the opponent. Appearing bigger in an agonistic
encounter is a valuable weapon for the individual, that might be able to end it before it
escalates to a more stressful and damaging physical dispute (Alcock 2005).
Fight is the last stage in an agonistic interaction between individuals, because of the
hight costs associated with the chances of loss and injuries. The ultimate consequence is the
death of an individual, what is extremely rare, but can happen (Richner 1985). Even so, fights
do occur among herons disputing resources, as food, territory and mates (Meyerriecks 1960,
Woolfeden et al. 1976, Forbes and McMackin 1984, Marion 1989, Nota 2003). Bayer (1984b)
has named as Face-off the interactions that lead to a fight between tow Great Blue Herons in
the foraging grounds. In all species, the actual fight occurs in a very similar way, as the birds
repeatedly lunge their bill and thrash their feet at one another, while beating the wings
60
rapidly. What differs between species is the display postures associated to the pre-fight period
(e.g. Wings-lined-up for the Little Blue Heron).
The territorial defense is common for herons during the nesting period, when the nest
and its surroundings are defended against other individuals. But true feeding territories are
few documented (Nota 2003, Yamada 1994, Marion 1989, Richner 1986, Recher 1972). In
the case of the Little Blue Heron in here, a true feeding territory is present; one that is fixed,
of exclusive use, and actively or passively defended against intruders (Moralez-Silva et al.
manuscrito 1).
A similar behavior to the Expulsion, the Pursuit Flight, was described by Bayer
(1984b). But this could occur in different interactions, as a territorial defense, a non-territorial
bird defending an individual distance, mobbing of predator or kleptoparasitism attempt.
Although a pursuit did occur for the Little Blue Heron in a defense of individual distance by
non-territorial herons and in a kleptoparasitism attempt, the use of pursuit on the Expulsion is
distinct, and occurs in a particular context. We have not observed any Little Blue Heron
pursuing individuals of another species. Therefore, we have not found necessary to
distinguish pursuit as a particular kind of interaction.
Although not in the context of territorial defense, the Great Egret and other species
presents an agonistic behavior during the breeding period in which the bird flies suddenly and
lands either atop its opponent or on the spot just vacated by the fleeing bird, often adopting an
extended neck posture, the Supplanting, as described by Mock (1978). As the Little Blue
Heron Expulsion, Supplanting is used to drive away undesirable individuals, and the use of an
extended neck might be related to a more aggressive outcome, since the normal flight is in the
S shape curved neck position.
The flight with an extended neck occurs too during the Circle Flight, displayed also
during the breeding period for various heron species. This behavior is considered as an
advertisement display (Mock 1976). So, another reason for the use of an extended neck during
61
the Expulsion might be related to an increase in the visibility of the individual, since
appearing bigger than it is, might drown the attention of the nearby birds.
The kleptoparasitism have been documented by various authors for different species of
herons and egrets (Collins 2006, Garrido et al. 2002, Lekuona 2002, González 1996, Kushlan
1978b). It occurs inter and intra-specifically for all those species, but a better understanding of
its dynamics and its role on the social context of foraging are not well understood. Garrido et
al. (2002) have suggested for the Cattle Egret, that this behavior serves to establish social
status among dominant individuals. For the Grey Heron (Ardea cinerea), Lekuona (2002) also
suggested that the kleptoparasitism could be a reflection of the social structure. Our
observations were not on individually marked herons, so we could not differentiate the use of
this behavior by distinct individuals in the aggregation. But we could observe that apparently,
only a few individuals expressed this behavior, suggesting the possibility of a role in the
social structure of Little Blue Heron feeding aggregated.
The agonistic behavior can be a real attack, or simply to involve threat behaviors, that is,
the postures and gestures that informs to the opponent to go away, or then, that it will became
an attack target (Kandel et al. 1995). Thus, the social interactions observed by us, including
the display postures, can be considered as been agonistic. In all of them, one of the
individuals is the “winner”, having a certain gain as the outcome of the dispute. Since these
interactions occur in the feeding site, during the foraging activities, we can assume that the
disputes are, direct or indirectly, over a food resource. One of the reasons for the territorial
defense might be the defense of an area with more food available (see Moralez-Silva et al.
manuscrito 1).
The social interactions between foraging herons are then diverse and very important in
defining the successful/unsuccessful use of the feeding resource, reflecting thus on the future
of the individual, its survival and reproduction.
62
Aknowledgements
This article represents part of a thesis submitted in partial fulfillment of the requirements for
the M.S. degree in the Departmento de Fisiologia, Universidade Federal do Rio Grande do
Norte, Rio Grande do Norte, Brazil. Finantial support, in form of a scholarship, is
acknowledged from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
(CAPES). Grateful thanks to the Instituto de Pesquisas Cananéia (IPeC) and its personnel for
furnishing equipments and physical support. And to friends and family, always important.
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Ajudando com a elaboração do projeto, assim como da dissertação e dos manuscritos,
contribuindo para a discussão dos resultados encontrados e suas relações com espectos
comportamentais e ecológicos. Esteve sempre presente, disponibilizando na forma de sua
pessoa ou do Instituto de Pesquisas Cananéia (IPeC), material bibliográfico e ajuda com a
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Tables and figures
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explaining any abbreviation used in that table. Footnotes to tables should be indicated by
superscript lower-case letters.
Illustrations must be restricted to the minimum needed to clarify the text. All figures
(photographs, graphs or diagrams) should be cited in the text, and numbered consecutively
throughout. Figure parts should be identified by lower-case roman letters (a, b, etc.). If
illustrations are supplied with uppercase labeling, lower-case letters will still be used in the
figure legends and citations.
Figure legends must be brief, self-sufficient explanations of the illustrations. The
legends should be placed at the end of the text.
69
Manuscrito 3
Título – Comportamento Territorial da Garça-azul, Egretta caerulea.
Autores - Emmanuel Moralez-Silva
1
, Flávio José de Lima Silva
2
and Emygdio Leite de
Araujo Monteiro-Filho
3
.
1
– Pós-Graduação em Psicobiologia – Estudos do Comportamento, Universidade Federal do
Rio Grande do Norte, Brazil. Instituto de Pesquisas Cananéia (IPeC), 199 Tristão Lobo,
Centro, Cananéia, SP, 11.990-000, Brazil.
2
- Laboratório de sistemática e Ecologia Animal, Dept. de Ciências Biológicas, Universidade
do Estado do Rio Grande do Norte. Mossoró-RN.
3
- Departamento de Zoologia, Setor de Ciências Biológicas, Centro Politécnico, Universidade
Federal do Paraná, PO Box 19020, Curitiba, PR, 81.531-990, Brazil. Instituto de Pesquisas
Cananéia (IPeC), 199 Tristão Lobo, Centro, Cananéia, SP, 11.990-000, Brazil.
Periódico – Ethology, QUALIS A.
Status – a ser submetido.
70
Resumo
O estabelecimento de um território para a defesa de uma área de alimentação, como
uma forma de utilização do habitat, pode ser o resultado de disputas que ocorrem em uma área
de forrageio na qual mais de um indivíduo utilizam os mesmos recursos, tendo assim uma
sobreposição de nicho entre eles. A utilização de territórios alimentares por garças e os
componentes comportamentais relacionados não foram documentados para muitas espécies.
Assim, este estudo vem para complementar o trabalho que vem sendo realizado sobre a
territorialidade alimentar da garça-azul, Egretta caerulea, em uma área de estuário no sudeste
do Brasil. O principal objetivo foi acessar o uso e a dinâmica de diferentes comportamentos
por indivíduos territoriais. Um indivíduo territorial utiliza primariamente três comportamentos
na manutenção de sua área, a Expulsão (freqüência - 13,74 ± 10,98), a Vocalização (9,53 ±
4,91) e o Encontro (1,66 ± 1,40). As flutuações diárias da maré mostraram-se tendo influência
no comportamento territorial da garça-azul, relacionando-se a exposição da área de
alimentação e a possibilidade ou não de intrusos adentrarem o território. A vocalização tem
aparentemente um forte componente social, a qual poderia ser utilizada para a proclamação da
posição de dominância que um indivíduo territorial ocupa no grupo. Todo o comportamento
social (soma dos três comportamentos) envolvido na manutenção de um território toma cerca
de 1,30% de todo o tempo gasto em um dia de atividade de forrageio. Aparentemente o
comportamento territorial da garça-azul não é muito custoso energeticamente, trazendo mais
benefícios do que gastos para o indivíduo. Todas as evidências apontam para a existência de
um indivíduo de garça-azul defendendo um território alimentar durante todo o período de
invernada, através de um comportamento territorial pouco custoso.
71
Title Page
Title – Little Blue Heron, Egretta caerulea, Territorial Behavior.
Authors - Emmanuel Moralez-Silva
1
, Flávio J. de Lima Silva
2
and Emygdio L. A. Monteiro-
Filho
3
.
1
– Programa de Pós-graduação em Psicobiologia – Estudos do Comportamento, Universidade
Federal do Rio Grande do Norte (UFRN), PO Box 1511, Natal, RN, 59078-970, Brazil.
Instituto de Pesquisas Cananéia (IPeC), 199 Tristão Lobo, Centro, Cananéia, SP, 11.990-000,
Brazil. E-mail: [email protected]. Corresponding author.
2
– Programa de Pós-graduação em Psicobiologia – Estudos do Comportamento, Universidade
Federal do Rio Grande do Norte (UFRN), PO Box 1511, Natal, RN, 59078-970, Brazil.
Laboratório de sistemática e Ecologia Animal, Dept. de Ciências Biológicas, Universidade do
Estado do Rio Grande do Norte, Mossoró, RN, Brazil. E-mail: [email protected].
3
– Departamento de Zoologia, Setor de Ciências Biológicas, Centro Politécnico,
Universidade Federal do Paraná, PO Box 19020, Curitiba, PR, 81.531-990, Brazil.
Instituto de Pesquisas Cananéia (IPeC), 199 Tristão Lobo, Centro, Cananéia, SP, 11.990-000,
Brazil. E-mail: [email protected].
Running title: Little Blue Heron Territorial Behavior.
Total number of words: 6.021
72
Abstract
The establishment of a territory to defend a feeding area, as one way of habitat use, can be the
outcome of disputes that occur in a feeding area where more than one individual use the same
resources, having then a niche overlap between each other. The use of feeding territories by
herons and egrets and the behavioral contents of it have not been documented for many
species. Therefore, this study comes as a complementary work on the feeding territoriality of
the Little Blue Heron, Egretta caerulea, in an estuarine area of southeastern Brazil, which
have been recently studied by these authors. The main objective was to access the use and
dynamics of different behaviors by territorial individuals. A territorial individual uses
primarily three behaviors in the maintenance of its area, Expulsion (frequency – 13.74 ±
10.98), Vocalization (9.53 ± 4.91) and Encounter (1.66 ± 1.40). The fluctuations of the tide
showed to have an influence in the Little Blue Herons territorial behavior, been related to the
exposition of the feeding area, and the possibility or not of intruders to enter the territory. The
vocalization has apparently a strong social component, which could be used to advertise and
proclaim the dominance position of a territorial individual in the group. The whole social
behavior involved in the maintenance of a territory (some of the three behaviors) accounts
only for about 1.30% of the time spent in the feeding site. Thus, it seams that the territorial
behavior in the Little Blue Heron dos not have such an energetic demand, bringing more
benefits than expenditures to the individual. All results point out to the existence of one Little
Blue Heron individual defending a feeding territory trough an entire winter, by a low cost
territorial behavior.
73
Introduction
The habitat selection is an important part of a species biology, and its consequences can rival
the impact of strong direct interactions among species in developing communities (Morin
1999). This selection is, thereafter, involved in the outcomes of the interactions of foraging
individuals in a determined area, and hence on the species use of habitat.
When more than one individual are exploiting the same resources, there is a niche
overlap between them, and a competition for the resource can arise. There are different
mechanisms in which this competition may arise; such as a simple exploitation of the same
resource, reducing the success rates of each bird; the scramble, in which every bird tries to be
the fastest in capturing the prey, without aggression; and the contest competition, where the
individuals interact aggressively to get the resource (Milinski & Parker 1991). The
competition leads to different distributions of the individuals in the different habitats. One of
the ways of resource use is by the defense of a portion of it, by defending the actual resource
or an area in which the resource is present. This is called despotic distribution, and some
individuals exclude others from a richer patch or habitat (Krebs & Davis 1997).
When an area is defended by one or more individuals, it is usually termed a territory.
There are different definitions for territory, but the one adopted here is the Maher and Lott’s
definition, that a territory is a fixed space from which an individual or group of mutually
tolerant individuals excludes competitors from a specific resource or resources (Maher & Lott
1995).
The knowledge of the behavioral dynamics of a species is currently considered as
fundamental to promote and maintain conservational actions to the preservation of a species
(Beissinger 1997). The behaviors related to the foraging activities directly affect the
individual’s chances of survival and reproduction. Therefore, and according to Tripp and
74
Collazo (1997), the identification of components of non-breeding territoriality of a species are
necessary to gain insights about its possible adaptive significance.
Although the knowledge of territories in the Ciconiiformes are well reported for the
nesting pairs, few species have had a true feeding territory reported; following the three
factors necessary to demonstrate territoriality by Brown and Orians (1970). Recently, the
existence of feeding territories for the Little Blue Heron, Egretta caerulea, have been reported
for a population that utilizes the rich estuarine-lagoon system of Cananéia, southeastern
Brazil, for foraging and living (Moralez-Silva et al. manuscrito 1). This species of heron is
poor studied in South America; and specifically in Brazil, only Olmos and its collaborators
have studied it, an mostly its reproductive ecology (Olmos et al. 2001; Olmos & Silva e Silva
2002). Thus, more profound studies on the behavior and ecology of its habitat use are
necessary for a better understanding of the species biology in this area of occurrence.
Therefore, the aim of this study was to characterize the behaviors associated to the territorial
defense in the Little Blue Heron, in the same area it have been studied by us since 2005:
identifying the frequency of occurrence of the behaviors uttered by territorial individuals, and
determining the frequency, latency and duration of those behaviors.
Methods
Study Area and Methods
The study was conducted in a mud bank in the estuarine-lagoon system of Cananéia,
southeastern coast of Brazil (from 25° 00` to 25° 04` S and 47° 54` to 47° 56` E) (Fig 1). The
system is formed by the islands Ilha de Cananéia, Ilha Comprida and Ilha do Cardoso.
Between these islands, there are channels that are connected to the open sea by the Barra de
Cananéia, between the Ilha Comprida and Ilha do Cardoso. The system is under the influence
of the tide. For a more detailed description of the area see Moralez-Silva et al. (manuscrito 1),
75
since this work is part of the results of a project been developed on the use of the habitat by
the Little Blue Heron in the region, been presented in different articles recently.
Figure 1. Map of part of the estuarine-lagoon system of Cananéia, Southeastern coast of
Brazil. The bold triangle indicates the mud bank used in the study of the territorial behavior of
the Little Blue Heron.
All data were collected from a single fixed point (an existing pier), from January to
August 2007. Since the individuals have not yet been marked, the only individuals that can be
monitored through an entire foraging period are the territorial ones. This because of there
fixed use of an exclusive and defended area. Therefore, the data were collected from the
individual (an adult, sex undetermined) defending the area in front of the observation point
(as described in Moralez-Silva et al. manuscrito 1). It had already been observed that this
individual remains the whole foraging period (of one day) defending this area, from its arrival
to its departure (Moralez-Silva et al. manuscrito 1). Thus, this individual could be monitored
for the entire foraging period, for several days, and its behaviors were taken note. The method
76
of focal sampling with continuous recording on a work sheet (Martin & Bateson 1993) was
used to the data collection.
The behaviors quantified are as described for the foraging Little Blue Heron in the area by
Moralez-Silva et al. (manuscrito 2). It was considered for this quantification the interactions
between individuals: 1. Expulsion; 2. Encounter; and 3. Kleptoparasitism; and also the Ahh-
ahh-ahh call (possible related to the social context) (from now on called vocalization). All
occurrences of these behaviors, for the territorial individual, were registered on a check-sheet
and chronometered. By this, true frequencies, durations and latencies of all behaviors were
accomplished.
Data Analysis
Two states of the tide were used in the analysis, described below:
1. Mud bank partially exposed – when the middle portion of the mud bank is covered.
2. Mud bank totally exposed – when the mud bank is completely exposed.
These items are related to an entire day of observation, so one day would be considered as
one or another. A total day category was also used to accomplish the total of days, grouping
the days of partially and totally exposed mud bank together.
To account for the distribution of the different behaviors in one day of foraging activity,
the days of mud bank totally exposed where subdivided into six periods of equal time
duration: from 1, the first period after the arrival of the territorial individual, to the subsequent
periods, until the last one, the 6.
To analyze the duration of the vocalizations (the Ahh-ahh-ahh call) as the time passed,
only the days with more then six vocalizations where used, to maintain enough variation
inside the category. Four categories where created: 1) First vocalization - the one
simultaneously with arriving; 2) Second vocalization – the second vocalization performed,
after the first; 3) Third vocalization – the next vocalization after the second; and 4) Following
vocalizations – all the other ones that came after the third (from three to 19).
77
All data were tested for normality by one-way Kolmogorov-Smirnov goodness-of-fit test
and for homocedascity by the F-max test (Zar 1999) before further tests were performed. In
general, the data had a normal distribution, but the variances were too different. Due to this,
and also to a small quantity of data for a few of the analysis, non-parametric tests were
chosen: Mann-Whitney (U) and Kruskal-Wallis one way ANOVA (H).
Pearson correlation was performed between the number of foraging individuals in the
mud bank per day and the frequency of occurrence of the Expulsion and the Vocalization,
also per day. Statistical significance was considered at α=0,05.
Results
Along 47 days of data collection, 224.17 hours of observation (mean ± SD: 05.16 ± 01.32
hours per day) were made, with the focal individual in sight. Of the 47 days, 33 were with the
mud bank totally exposed, and 14 were with the mud bank partially exposed.
The territorial individual arrived as soon as the day cleared (06.24 ± 00.24 in the
morning), and landed in the mangrove trees in the margin of its territory when the tide was
still high, or directly on the ground when the tide was lowering, and a few mud was already
exposed. This individual was always one of the first individuals to arrive at the area, coming
from the roosting area, about one kilometer northern, in a mangrove island. But it was
observed to arrive latter some times, even as the number 37 once. Another two territorial
individuals would also arrive almost at the same time, and land on its respective territories
(one to northern and the other to southern, but yet neighbors of the territorial). All the other
individuals would land to southern, on an exposed area (when the mud bank was still
covered), or directly on the mud bank, when exposed. It was never observed another
individual landing on the territorial area before this had arrived, and also this has never landed
on another ones area. After the territorial had arrived on its area, if other individual would try
to land, it would be expelled; but this was uncommon. The usual intrusion would happen
78
during the mud bank exposed time, by walking. The territorial individual was observed
landing on the ground as it arrived, and immediately start foraging, or waiting up to 156 min
to land on the ground and start foraging, when arriving with the high tide.
There were a total of 640 expulsions, 451 vocalizations, and 77 encounters registered
during the study period. Of the expulsion, 88.59% where without the vocalization associated,
and the other 11.41% had the vocalization associated. The expulsion without the vocalization
occurred on average 14.18 ± 9,82 times per day, and with the vocalization associated occurred
on average 1.89 ± 1,60 times per day. The vocalization alone occurred in the arrival of the
territorial individual and after a short flight within its territory. The encounter occurred most
times with the two territorial neighbors.
When the mud bank was partially exposed, the vocalization had a greater frequency
(7.60 ± 3.72) then the other two behaviors (expulsion – 3.20 ± 2.37; encounter – 1.60 ± 1.35)
(H=20.60, GL=2, p<0.01) (Fig. 2a). In the mud bank totally exposed condition, the frequency
of occurrence of the expulsion was higher (18.69 ± 9.87), followed by the vocalization (10.44
± 5.19) and then by the encounter (1.69 ± 1.45) (H=70.31, GL=2, p<0.01) (Fig. 2b). Now,
when grouping them into the total day category, the expulsion (13.74 ± 10.98) and the
vocalization (9.53 ± 4.91) had a similar frequency of occurrence, been this higher then the
frequency of encounter occurrence (1.66 ± 1.40) (H=70.90, GL=2, p<0.01) (Fig. 2c).
Significant differences between the two tidal conditions occurred only for the expulsion,
which presented a higher frequency in the totally exposed mud bank condition (U=1.50,
p<0.01) (vocalization – U=168.00, p=0.13; encounter – U=200.50, p=0.48).
79
A
Expul.
Vo
cal.
Encount.
0
5
10
15
20
Number of behavior / day
B
Expul.
Vocal.
Encount.
0
10
20
30
40
50
Number of behavior / day
C
E
xpul.
V
ocal
.
En
c
o
u
nt.
0
10
20
30
40
50
Number of behavior / day
Figure 2. Frequency of the behaviors of a territorial Little Blue Heron, in a mud bank in the
Cananéia estuary, Brazil. (a) mud bank partially exposed; (b) mud bank totally exposed; (c)
total day category. Values are given as median, with the whiskers representing minimum to
maximum value.
In both conditions (partially exposed mud bank – H=88.50, GL=2, p<0.01; totally
exposed mud bank – H=524.57, GL=2, p<0.01), as well as in the total day category
(H=630.81, GL=2, p<0.01), the duration of the encounter (partially exposed – 46.35 ± 40.88s;
totally exposed – 34.63 ± 32.73; total day – 39.00 ± 36.17) was very higher then the other two
behaviors, followed by the expulsion (partially exposed – 9.96 ± 9.24; totally exposed – 8.75
± 5.65; total day – 8.85 ± 6.02) and then by the vocalization (partially exposed – 3.18 ± 1.69;
80
totally – 2.85 ± 1.76; total day – 2.95 ± 1.74) (Figs. 3a,b,c). The duration of the expulsion
(U=11433.50, p=0.62), the encounter (U=520.00, p=0.16), and the vocalization (U=13056.00,
p=0.51) showed no significant differences between the two tidal conditions (totally and
partially exposed mud bank) (Figs. 3a,b).
A
Expul.
V
o
ca
l
.
Encount.
0
50
100
150
200
Time (s)
B
Ex
p
u
l.
Vocal
.
E
nc
ount.
0
50
100
150
200
Time (s)
C
Expul.
V
oc
al
.
Enc
ount.
0
50
100
150
200
Time (s)
Figure 3. Duration of the behaviors of a territorial Little Blue Heron, in a mud bank in the
Cananéia estuary, Brazil. (a) mud bank partially exposed; (b) mud bank totally exposed; (c)
total day category. Values are given as median, with the whiskers representing minimum to
maximum value.
The vocalization was the only behavior that occurred simultaneously with arrival, in
100% of the days, having then a latency of 0. The latency for the other two behaviors
(expulsion: partially exposed mud bank – 77.50 ± 47.68 min; totally exposed mud bank –
81
65.18 ± 37.52; total day category – 68.47 ± 40.28 / encounter: partially exposed – 93.91 ±
52.92; totally exposed – 107.83 ± 65.68; total day – 103.32 ± 61.38) did not differ between
the two tidal conditions (expulsion – U=159.00, p=0.66; encounter – U=104.00, p=0.62) (Fig.
4a,b); and the encounter had a slightly higher latency then the expulsion in general (totally
exposed – U=292.50, p<0.05; total day – U=549.50, p<0.05), only not in the partially exposed
mud bank condition (U=38.50, p=0.59) (Figs. 4a,b,c).
A
E
x
pu
l
.
Vocal.
Encount
.
0
50
100
150
200
250
Time (min)
B
E
xpu
l
.
V
o
c
a
l.
Encount.
0
50
100
150
200
250
Time (min)
C
E
x
pul.
V
oca
l
.
Encount.
0
50
100
150
200
250
Time (min)
Figure 4. Latency of the behaviors of a territorial Little Blue Heron, in a mud bank in the
Cananéia estuary, Brazil. (a) mud bank partially exposed; (b) mud bank totally exposed; (c)
total day category. Values are given as median, with the whiskers representing minimum to
maximum value.
82
In the partially exposed mud bank condition, there was no difference in the time
interval between the occurrences of the behaviors between the expulsion (38.70 ± 43.52 min)
and the vocalization (26.25 ± 23.55) (U=1599.00, p=0.74) (Fig. 5a). Yet, statistically
significant differences occurred between the expulsion (8.41 ± 9.63) and the vocalization
(25.79 ± 27.28) for the totally exposed mud bank condition (U=41612.00, p<0.01) (Fig. 5b);
and also for all three behaviors when grouping them into the total day category (expulsion –
9.68 ± 14.21; vocalization – 25.89 ± 26.46; encounter – 62.51 ± 58.15) (H=207.50, GL=2,
p<0.01) (Fig. 5b). The time interval differed statistically between the two tidal conditions for
the expulsion (U=3819.00, p<0.01), but not for the vocalization (U=15032.00, p=0.51) (Fig.
5a). Since there were few data, and a very variable one (VAR=3166.85; CV=95.46) for the
encounter, this behavior was excluded from the analysis of the tidal conditions, been included
only in the total day category analysis.
A
E
xpul
.
Vocal.
E
xpul.
V
ocal.
0
50
100
150
200
Partially exp. Totally exp.
Time (min)
B
Exp
u
l.
V
oc
a
l
.
E
n
c
oun
t
.
0
100
200
300
Time (min)
Figure 5. Time intervals between the occurrences of the behaviors of a territorial Little Blue
Heron, in a mud bank in the Cananéia estuary, Brazil. (A) mud bank partially exposed, and
totally exposed; (B) total day category. Values are given as median, with the whiskers
representing minimum to maximum value.
83
The duration of the first vocalization (6.90 ± 1.42 s) was greater then the second (4.04
± 1.40), the third (2.69 ± 0.78) and the followings (2.26 ± 0.92) (H=138.56, GL=3, p<0.01)
(Fig. 6).
F
irst
S
e
cond
Thir
d
Fol
l
ow
.
0
5
10
15
Time (s)
Figure 6. Duration of the vocalizations of a territorial Little Blue Heron, throughout a
foraging day in a mud bank in the Cananéia estuary, Brazil. Values are given as median, with
the whiskers representing minimum to maximum value.
The expulsion occurred more in the middle portion of on day of foraging activity
(H=79.23, GL=5, p<0.01). The vocalization occurred more in the initial portion of one day
(H=26.35, GL=5, p<0.01). No significant differences were found for the encounter, occurring
homogeneously though one day of foraging activity (H=3.91, GL=5, p=0.56) (Fig. 7).
84
1
2
3
4
5
6
0
2
4
6
8
10
Expul.
Vocal.
Encount.
Periods of time
Number of behavior / period of time
Figure 7. Distribution, in one foraging day (divided into six periods of equal time), of the
behaviors of a territorial Little Blue Heron, in a mud bank in the Cananéia estuary, Brazil.
Values are given as mean ± SE.
In table 1 are the percentage of the time each behavioral unit occupied in the feeding
time of one day of foraging activity. The expulsion amount of time is significantly higher than
the other two behaviors (H=29.60, GL=2, p<0.01).
Table 1. The times and percentages of time each behavioral unit occupied during one day of
foraging activity of the Little Blue Heron in the Cananéia estuary. The total column is the
some of the three units and the relation of time they occupied in one day of foraging activity.
Behavioral
units
Expulsion Vocalization Encounter Total (some)
time (s) % time (s) % time (s) % time (s) %
85
A weak correlation was found between the number of Expulsions (13.74 ± 10.98) and
the number of individuals (50.4 ± 13.99) foraging in the mud bank in one day of activity
(r=0.34, GL=45, p=0.036). A more strong correlation was found between the number of
individuals foraging and the number of vocalizations (9.53 ± 4.91) in one day of activity
(r=0.60, GL=45, p<0.01).
Discussion
The influence of the tide on the territorial behavior of the Little Blue Heron became clear, and
can be observed in almost all the analysis where tide is a variable. What can be observed is
that the use of the vocalization is more related to the initial portion of the foraging time, the
period where normally the tide is lowering. This is probably because the presence of an
intruder on the territorial individual’s area it is not required for the execution of this behavior,
since the intruders would normally intrude by walking. Now, the expulsion depends on the
existence of an intruder on the territorial individual’s territory, and so, it can be observed that
the frequency of this behavior is higher in the periods of exposed mud bank, and thus,
consequently, the time intervals between its occurrences are lower in this period.
There seams to be a tread between these two behaviors, from the beginning to the end
of the foraging periods, been the vocalization used more in the initial/middle portion and the
expulsion more in the middle/final portion. This suggests that they are both important in the
territorial maintenance, and can be used for the same purpose at different times of the
individuals foraging activity budget.
Only the encounter had no differences concerning the different tidal conditions, and
this is probably due to the fact that the encounter happened normally between the territorial
individual and another territorial neighbor. These neighbors where present independently of
the tide, so the encounter could happen at any time.
86
The only parameter that the tide seams not to influence is the duration of the
behaviors, and this appears to be plausible, since the dynamics of the tide are not so drastic,
happening in a greater time scale then the behaviors.
The physical environment affects the lives of ciconiiforms in different aspects, such as
in form of the hydrological conditions, which can switch in dramatic ways between seasons;
and have a strong relation to, for example, the nesting phenology of a species (Kushlan 1981).
In a more restrict scale, the influence of the tidal cycle on the individual’s behaviors, and its
influences on the use and distribution on the habitat of different species have been
documented by various researchers (Custer & Osborn 1978; Rodgers 1983; Richner 1986;
Bryan et al. 2002; Maccarone & Brzorad 2005; Swennen & Yu 2005).
The vocalization, as suggested earlier by us (Moralez-Silva et al. manuscrito 2),
apparently has a strong social component. It is used mainly as an exclusive behavior, that is,
not associated to the expulsion; and also, most in the beginning and middle portion of the
foraging period. The first vocalization, when arriving at the site, is the one that lasts the most;
and the second have also a bigger duration them the following ones. Therefore, this particular
call might be one of the forms to advertise and proclaim the dominance position of a
territorial individual. Also, the vocalization could be used as a way to avoid further confront
between individuals; further danger of injury and waist of important energy reserves. The
positive correlation found between the number of individuals foraging in the mud bank in one
day and the number of vocalizations given in one day is another result that points out to this
direction. As suggested earlier by us (Moaralez-Silva et al. manuscrito 2), this vocalization
could be homologous to the Roh-roh-roh call of territorial feeding Great Blue Herons (Bayer
1984); which, according to Bayer (1984), could be used as a distinguishable call between
territorial neighbors, helping to identify strangers and minimize interactions with neighbors.
The use of a vocalization or song in context disputes over territories is not uncommon, and it
has been associated to the signaling of aggressiveness between rivals for various species of
87
birds (Kroodsma & Byers 1991; Aubin et al. 2004; Searey et al. 2006; Ripmeester et al.
2007), and also for amphibians (Bee & Gerhardt 2002) and insects (Mason 1996).
We have suggested earlier (Moralez-Silva manuscrito 2) that the intraspecific
kleptoparasitism could be acting on the social organization of the foraging Little Blue Heron;
as it was suggested for the Cattle Egret, Bubulcus ibis, in which this behavior could be serving
to establish social status among dominant individuals (Garrido et al. 2002). But, since no
kleptoparasitism was observed for the territorial individual, this might not be the case in here.
Yet, this behavior is observed for the specie in the area. Thus, the use of this behavior in the
social context should not be discredited; it could be acting in this context in a different
manner. Therefore, further study is needed to establish the function of this behavior in the
social foraging of the Little Blue Heron.
The expulsion accounts for more then 50% of the time spent in the social behaviors.
The vocalization and the encounter account for about 15% each (this can also be seen in the
frequencies of each behavior’s use). Thus, the active defense of the resource appears to have a
stronger part on the individual’s choice and time budget. The vocalization and the encounter
might serve more as advertisement displays of the individual’s dominance to its co specifics.
According to Stamps and Krishnan (1994), territory owners dominate floaters and
subordinates. Therefore, the actual defense of the territory seams to be made by the active
defense, and the other social behaviors completes the proclamation of the dominance position
that the retention of a defended area brings to the individual.
However, the whole social behavior (some of the three behaviors) involved in the
maintenance of a territory accounts only for about 1.30% of the time spent in the feeding site,
in foraging activity. Similar results were found for wintering Pied Wagtail (Motacilla alba
yarrellii), spending about 4% of the time on each foraging day on defense related behaviors
(Davis 1976). Thus, the defense of this area, one that could bring greater foraging benefits to
the individual feeding on it (Moralez-Silva et al. manuscrito 1), does not appears to have such
88
an energetic demand to the territorial individual. It can be assumed that the expulsion (active
defense) has more energetic expenditures than the vocalization and the encounter, each also
having a lower frequency of occurrence. Therefore, the territorial behavior might be a good
strategy for the individual, one that can bring great benefits with low costs. These costs are
not minimal as in some species that follow some very simple movement rules in the
population; such as Pararge aegeria, the Speckled Wood Butterfly, in which the intruding
males retreat on perceiving that a territory is occupied (Davies & Houston 1984). But the
costs appear to be very low, different from other species. In some species of water birds that
exhibits feeding ground territoriality, the costs associated to the maintenance of the territory
are much greater. Trippi and Collazo (1997) have found for Semipalmated Sandpipers that
territory holders do have nearly exclusive access to higher than average prey concentrations;
but to gain this privilege, they spent large amounts of time, up until 67% of the foraging time,
on aggression and vigilance behaviors. For other species of birds, the costs of defense can
also be as heavy (e.g. Davis & Houston 1984; Temeles et al. 2005). Therefore, this reinforces
the defended territory as an economically defendable site (Moralez-Silva et al. manuscrito 1).
Yet, these social behaviors can also be considered to be received by more than one
individual (receiver) at a time. The sound in a more direct way, since it is of long range; but
the encounter and the expulsion could also be eavesdropped by an individual other then the
intended receiver (McGregor 1993). This could be helping a territorial individual in the
maintenance of its territory with less need of use of those behaviors; and thus, less energy
loss, with more time for foraging.
Davis and Houston (1984) point out for three main factors that will influence the
economic defendability of a resource: i) resource quality and distribution in space; ii) resource
distribution in time; and iii) competition for the resource. In a previous work, we had some
results that might suggest that the defense of a feeding territory in the Little Blue Heron is
more related to the distribution of the resource in space than to the competition for this
89
resource (Moralez-Silva et al. manuscrito 1). Our results in here reinforce this assumption.
The frequency of defense related behaviors are low, accounting for very little portion of the
individuals for i.sasng
90
Therefore, the apparent low cost defense of a beneficial feeding territory by one
individual trough an entire feeding winter can be the case for the Little Blue Heron in the
Cananéia estuary.
Acknowledgments
This article represents part of a thesis submitted in partial fulfillment of the requirements for
the M.S. degree in the Departamento de Fisiologia, Universidade Federal do Rio Grande do
Norte, Rio Grande do Norte, Brazil. Finantial support, in form of a scholarship, is
acknowledged from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
(CAPES). A grateful thanks to the Instituto de Pesquisas Cananéia (IPeC) and its personnel
for furnishing equipments and physical support. And to friends and family, always important.
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O autor Emygdio L. A. Monteiro-Filho colaborou desde o início do trabalho, no ano de 2005.
Ajudando com a elaboração do projeto, assim como da dissertação e dos manuscritos,
contribuindo para a discussão dos resultados encontrados e suas relações com espectos
comportamentais e ecológicos. Esteve sempre presente, disponibilizando na forma de sua
pessoa ou do Instituto de Pesquisas Cananéia (IPeC), material bibliográfico e ajuda com a
logistica do trabalho de campo.
94
Ethology – Formatação.
Content
The Abstract should introduce the topic, the main objective, the main result(s) and the
principle conclusion(s). The Introduction should explain the main questions addressed in the
paper. Continuity with earlier work on the subject should be established by reference to recent
papers or reviews, which need not themselves be summarized. Experimental methods must be
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References
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Greenfield, M. D. & Rand, A. S. 2000: Frogs have rules: selective attention algorithms
regulate chorusing in Physalaemus pustulosus (Leptodactylidae). Ethology 106, 331-347.
Zar, J. H. 1996: Biostatisitcal Analysis, 3rd edn. Prentice Hall, Engelwood Cliffs, New Jersey.
Johnstone, R. A. 1997: The Evolution of Animal Signals. In: Behavioural Ecology, 4th edn
(Krebs, J.R. & Davies, N. B., eds). Blackwell Science, Oxford, pp. 155-178.
Schütz, D. 1998: Sexual size dimorphism in a shell-brooding cichlid Lamprologus callipterus.
Ph.D. Thesis, Ludwig-Maximilian-Universität, Munich, Germany.
Articles not yet published may only be cited if their place of publication is certain.
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Discussão/Conclusão Geral
Segundo Brown & Orians (1970), para se demonstrar a existência de um território em
uma dada espécie, é necessário observar/demonstrar três fatores simultaneamente: um
97
Meyerriecks 1960). As outras duas são novas na literatura. Uma é a postura Estendida (ou
“Extended”) e a outra é a postura Asas-alinhadas (ou “Wings-lined-up”). Dentre os Ardeidae,
é considerado que as posturas de exibição evoluíram como parte do repertório comunicativo
dos indivíduos, agindo no canal visual de comunicação entre indivíduos (Mock 1976). As
posturas registradas não são utilizadas em um contexto solitário, elas são utilizadas nas
interações entre indivíduos. Todas as posturas de exibição, assim como as interações entre
indivíduos observadas no presente trabalho, são utilizadas em um contesto agonístico;
considerando-se agonístico o comportamento que pode ser um ataque real, ou simplesmente
envolver comportamentos de ameaça, posturas e gestos (Kandell et al. 1995). Desta forma,
estas interações derivam de disputas, as quais são travadas dentro da área alimentar, levando a
uma boa vantagem para o “vencedor” destas disputas, um acesso mais exclusivo do recurso
alimentar.
Um indivíduo de garça-azul territorial utiliza-se então destes comportamentos para a
defesa de uma área exclusiva dentro do habitat alimentar. O conceito de “defesa econômica”
(“economic defendability”) proposto por Brown (1964) diz que somente esperaríamos que um
animal gastasse tempo e energia interagindo com outros para defender um território se este
comportamento trouxesse mais benefícios líquidos do que outro comportamento alternativo
(Davis & Houston 1984). No presente estudo, foi observado que a área defendida (uso
exclusivo) pelo indivíduo territorial é maior do que a área média restante para cada um do
restante de indivíduos forrageando no baixio; além de ser em uma área que traz maior sucesso
de forrageio, com menores gastos. Ainda, foi também observado que o tempo gasto com os
comportamentos relacionados à defesa, pelo indivíduo territorial, ocupa apenas, em média,
1,30% do tempo gasto em um dia de atividade de forrageando na área. Outras espécies que
apresentam comportamento territorial passam muito mais tempo em comportamentos de
defesa e tem custos de defesa bem mais pesados (Temeles et al. 2005, Tripp & Collazo 1997,
Davis & Houston 1984). Assim, o comportamento territorial da garça-azul aparentemente tem
um custo baixo em relação aos benefícios que traz para o indivíduo; caso contrário não teria
sido selecionado durante o processo evolutivo.
O ambiente físico afeta as vidas dos Ciconiiformes de variadas formas, desde
mudanças em curto prazo das condições climáticas até mudanças sazonais, especialmente dos
recursos alimentares (Kushlan 1981). Mudanças locais, mais restritas, como as variações
diárias da maré, em ambientes costeiros, também têm influência nos comportamentos destas
aves, influenciando assim a utilização do habitat (Maccarone & Brzorad 2005, Yu &
Swennen 2004, Bryan et al. 2002, Richner 1986, Rodgers 1983, Custer & Osborn 1978). No
presente estudo pode-se verificar que a maré também tem influência sobre o comportamento
98
territorial da garça-azul, intervindo na utilização dos diferentes comportamentos relacionados
à defesa, principalmente a expulsão e a vocalização.
Destes comportamentos, a expulsão teve maior freqüência de ocorrência, no geral, do
que a vocalização e o encontro; assim como ocupou, em média, 50% de tempo gasto nestes
comportamentos. Desta forma, é possível que a defesa territorial seja utilizada principalmente
para a defesa ativa, enquanto que os outros dois comportamentos sirvam mais como aviso e
sinalização da posição de dominância que o indivíduo territorial ocupa no grupo. Segundo
Stamps & Krishnan (1994), indivíduos territoriais dominam os não-territoriais do grupo. O
uso de vocalizações e cantos em disputas territoriais não é incomum, tendo sido observado
nas interações territoriais de várias espécies, não somente de aves (Searey et al. 2006, Aubin
et al. 2004, Bee & Gerhardt 2002, Mason 1996). Para a garça-azul, observou-se no presente
estudo que a vocalização é realizada em uma baixa freqüência de amplitude, ou seja, alto
potencial de dispersão no ambiente, principalmente em um ambiente aberto; é utilizada
principalmente por indivíduos territoriais; é utilizada principalmente como um
comportamento exclusivo, ou seja, não associado ao comportamento de expulsão; e as
primeiras vocalizações do indivíduo territorial ao chegar no baixio duram significativamente
mais tempo do que as do restante do período de forrageio. Desta forma, aparentemente esta
vocalização (o chamado Ahh-ahh-ahh) em particular é importante no contexto social do
forrageio para a espécie. Sendo um comportamento que pode estar ajudando o indivíduo
territorial a proclamar e manter sua posição de dominância no grupo.
A dinâmica comportamental da utilização do habitat alimentar de uma espécie é uma
de suas características de grande valor para o entendimento de sua biologia; principalmente
quando se olha para o quadro de conservação e preservação atual. Os comportamentos
relacionados às atividades de forrageio afetam diretamente as chances de sobrevivência e
reprodução de um indivíduo, atuando sobre o processo de seleção natural deste. Segundo
Beissinger (1997), o conhecimento das dinâmicas comportamentais de uma espécie é
atualmente considerado fundamental para promover e manter ações de conservação para a
preservação da espécie. Ainda, de acordo com Tripp & Collazo (1997), a identificação de
componentes da territorialidade não-reprodutiva de uma espécie é necessária para um futuro
entendimento de sua possível significância adaptativa. O presente trabalho traz novos e
importantes aspectos do comportamento de uma espécie bastante conhecida, porém pouco
estudada na América do Sul; reforçando a importância das interações sociais de indivíduos
forrageando em grandes grupos, em áreas de alto valor ecológico.
Palmer (1962) observou, para a garça-azul, indivíduos defendendo vigorosamente
territórios alimentares fora do período reprodutivo. Isto é pouca informação para afirmar a
99
real existência de territórios alimentares para a espécie. Porém, com os resultados
apresentados neste trabalho, reforça-se a concepção desta existência.
Nossos resultados mostraram que em um dia de observação o indivíduo defendendo
um território no baixio é sempre o mesmo, visto que este chegava à área no inicio do período
alimentar e permanecia até seu final. Este indivíduo, embora não marcado para identificação
individual, parece ser sempre o mesmo durante todo o período do estudo. Este era sempre um
dos primeiros a chegar à área, pousando sempre dentro da mesma área (seu território). Mesmo
não sendo o primeiro indivíduo a chegar ao baixio, seu território nunca era ocupado por outro
individuo que não ele próprio. Outros indivíduos eram observados tentando pousar em seu
território, mas sempre após a sua chegada. Ainda, o indivíduo territorial foi observado
esperando até 156 min, empoleirado no mangue, antes de poder começar a forragear. Assim, a
aparente defesa pouco custosa de um território alimentar por um único indivíduo por um
período de invernada inteiro parece ser o caso da garça-azul no estuário de Cananéia.
As interações sociais entre garças forrageando são, então, diversas e bastante
importantes na definição do sucesso/insucesso no uso do recurso alimentar, refletindo assim
no futuro do indivíduo, sua sobrevivência e reprodução.
100
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