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INSTITUTO NACIONAL DE PESQUISAS DA AMAZÔNIA - INPA
UNIVERSIDADE FEDERAL DO AMAZONAS - UFAM
PROGRAMA INTEGRADO DE PÓS-GRADUAÇÃO EM BIOLOGIA TROPICAL E
RECURSOS NATURAIS DA AMAZÔNIA
COMPONENTES QUANTITATIVO E QUALITATIVO DO SISTEMA PLANTA-
POLINIZADOR DE Psychotria brachybotrya (RUBIACEAE) E Tabernaemontana
undulata (APOCYNACEAE) NO SUB-BOSQUE DE FLORESTA PRIMÁRIA NA
AMAZÔNIA CENTRAL.
THAYSA NOGUEIRA DE MOURA
MANAUS, AMAZONAS
MAIO, 2008
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THAYSA NOGUEIRA DE MOURA
COMPONENTES QUANTITATIVO E QUALITATIVO DO SISTEMA PLANTA-
POLINIZADOR DE Psychotria brachybotrya (RUBIACEAE) E Tabernaemontana
undulata (APOCYNACEAE) NO SUB-BOSQUE DE FLORESTA PRIMÁRIA NA
AMAZÔNIA CENTRAL.
ORIENTADOR: ANTONIO CARLOS WEBBER
Dissertação apresentada ao
Programa de Pós-graduação em Biologia
Tropical e Recursos Naturais do
convênio INPA/UFAM, como parte dos
requisitos para obtenção do título de
Mestre em Botânica.
MANAUS, AMAZONAS
MAIO, 2008
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Ficha Catalográfica:
M929 Moura, Thaysa Nogueira
Componentes quantitativo e qualitativo do sistema planta-polinizador de
Psychotria brachybotrya (Rubiaceae) e Tabernaemontana undulata
(Apocynaceae) no sub-bosque de floresta primária na Amazônia Central/
Thaysa Nogueira de Moura.--- Manaus : [s.n.], 2008.
43f. : il.
Dissertação (mestrado) --- INPA/UFAM, Manaus, 2008
Orientador : Antonio Carlos Webber
Área de concentração : Botânica
1. Polinização. 2. Efetividade do polinizador. 3. Variação espacial
(Botânica). 4. Florestas tropicais – Amazônia. I. Título.
CDD 19. ed. 582.01662
Sinopse:
Estudou-se o sistema de polinização de duas espécies do sub-bosque de floresta
primária em duas áreas próximas à cidade de Manaus, Amazonas. Variação na taxa
de visitação, abundância relativa e na efetividade na polinização foram avaliadas
entre as espécies de visitantes florais.
Palavras-chave:
Polinização, efetividade da polinização, taxa de visitação, abundância relativa, sub-
bosque, Amazônia Central.
AGRADECIMENTOS
Agradeço às seguintes pessoas cujo apoio, direta ou indiretamente, tornou possível a
realização desta dissertação: Prof. Dr. Antonio Carlos Webber (INPA/UFAM), Dr. Jeff
Ollerton (University of Northampton), Prof. Dr. Marco Antonio de Freitas Mendonça
(Coordenador da Fazenda Experimental – UFAM), Prof. Dr. Thierry Gasnier (INPA/UFAM),
Dra. Flavia Costa (INPA), Sr. Francisco (Transportes – UFAM), Sr. Laudelino (motorista –
UFAM), Sra. Neide e Sra. Gisele (Secretaria Botânica – INPA), Sr. Deisivaldo (mateiro –
Fazenda Exp. UFAM) e a todos os funcionários da Faz. Exp. da UFAM. Agradeço muito
especialmente às amigas Eunice e Liliane Noemia Torres de Melo (minha fiel companheira de
campo). O projeto foi desenvolvido no Instituto Nacional de Pesquisas da Amazônia, em
convênio com a Universidade Federal do Amazonas. A bolsa de mestrado foi concedida pelo
CNPq.
RESUMO
Variação na efetividade da polinização e na freqüência de visitas entre os visitantes florais
representa uma oportunidade para plantas se especializarem nas espécies que conferem o
melhor serviço de polinização. No entanto, fatores ambientais, como efeitos locais, podem
determinar a imprevisibilidade espaço-temporal na composição da assembléia dos
polinizadores, limitando as possibilidades para a coevolução. A variação na efetividade da
polinização e taxa de visitação foi investigada entre os visitantes florais de duas espécies de
sub-bosque em floresta primaria: Psychotria brachybotrya (Rubiaceae) e Tabernaemontana
undulata (Apocynaceae). No sistema de polinização de P. brachybotrya não foram
encontradas diferenças quanto à efetividade de polinização e na abundância relativa entre as
três espécies de abelhas que atuaram como polinizadores da espécie. A similaridade nos
componentes quantitativo e qualitativo da interação entre as três espécies de visitantes florais
reduz as possibilidades de especialização de P. brachybotrya. As flores de T. undulata
possuem características da síndrome de polinização por mariposas, mas por permanecerem
receptivas ao longo do dia, ofertando néctar e emitindo intenso odor floral, são visitadas por
duas espécies de abelhas Euglossine. Através do uso de medidas diretas da efetividade da
polinização foi possível comprovar que pelo menos uma das espécies de visitante floral é
capaz de transferir pólen e efetivar a polinização. O uso de medidas indiretas da efetividade
do polinizador, como a contagem de grãos de pólen depositados sobre o estigma após visita, é
indispensável em futuros estudos para esclarecer o papel desempenhado pelos visitantes
florais diurnos na polinização de T. undulata.
ABSTRACT
Variation in pollination effectiveness and frequency of visits among flower visitors represents
an opportunity for plants to specialize on taxa providing the best pollination services.
However, environmental factors, such like site-specific effects, may determine spatiotemporal
unpredictability in the composition of pollinator assemblages, limiting possibilities for taxon-
specific coevolution. We investigated the variation in pollination effectiveness and visitation
rate among the flowers visitors of two understory species in primary forest: Psychotria
brachybotrya (Rubiaceae) and Tabernaemontana undulata (Apocynaceae). In the P.
brachybotrya pollination system, we did not find significant differences in pollinator
effectiveness and frequency of visits among the three bee species. The similarity in the
quantity and quality components of interaction among the three floral visitor taxa reduces the
possibilities of specialization of P. brachybotrya on any of these bee species. The flowers of
T. undulata show characteristics of the moth-pollination syndrome, but because they are
receptive throughout the day, offering nectar and emitting an intense floral odor, they are
visited by two Euglossine species by the morning. Through the use of direct measures of the
pollinator effectiveness we could show that at least one bee species is able to transfer pollen
and promote pollination. The use of indirect measures of pollination effectiveness in future
studies, such as quantifying the amount of pollen grains deposited on the stigma after visits is
indispensable to clarify the role of the diurnal flower visitors in T. undulata pollination.
SUMÀRIO
INTRODUÇÃO GERAL 1
CAPÍTULO 1 7
Similarity in pollination effectiveness among the three floral visitors of Psychotria brachybotrya
(Rubiaceae) in the understory of primary forest in Central Amazonia, Brazil.
CAPÍTULO 2 24
Floral biology and pollinator effectiveness of the diurnal floral visitors
of Tabernaemontana undulata Vahl. (Apocynaceae)
in the understory of Amazon Rainforest, Brazil.
.
CONCLUSÃO 40
REFERÊNCIAS BIBLIOGRÁFICAS 41
1. INTRODUÇÃO
Grande parte das Angiospermas apresenta interações com uma vasta gama de
visitantes florais, sendo alguns destes capazes de efetivar a polinização. O espectro de
polinizadores de uma planta pode variar desde ordens até mesmo classes de animais (Ollerton,
1996; Waser et al., 1996). A gama de visitantes e polinizadores freqüentemente varia espacial
e temporalmente. Além disso, condições microclimáticas diversas podem afetar a composição
dos polinizadores entre indivíduos de uma mesma espécie de planta (Herrera, 1995; Ollerton,
1996).
Ainda sim, supõe-se que a evolução da diversidade floral seja baseada nas relações
especializadas entre espécies de plantas e polinizadores, noção essa que levou à categorização
das plantas com flores nas síndromes de polinização (Faegri e Pijl, 1979). Porém, estudos
evidenciam que mesmo plantas com características de uma determinada síndrome podem ser
visitadas por diferentes organismos que contribuem na polinização em algum grau (Spears,
1983; Waser et al., 1996). Além disso, muitos dos organismos que visitam uma população de
plantas podem não ser agentes polinizadores, mas pilhadores de pólen e néctar, não
contribuindo para sua reprodução (Spears, 1983).
Ollerton (1996) destacou o aparente paradoxo entre os processos ecológicos e os
padrões filogenéticos, onde muitas flores apresentam traços florais especializados, ao mesmo
tempo em que são visitadas por diversos visitantes florais (Johnson e Steiner, 2000). Uma das
possíveis explicações propostas por Ollerton (1996) para o aparente paradoxo é a de que
dentre todos os visitantes florais que uma espécie de planta recebe apenas alguns atuam
efetivamente na polinização. Este autor sugere que tal diferença na habilidade da polinização
entre diferentes visitantes florais provavelmente seja algo comum na natureza, mas que vem
sendo pouco estudado.
Diferenças entre visitantes florais com relação à morfologia, fisiologia e
comportamento podem resultar em diferenças quanto à efetividade na polinização (Schemske
e Horvitz, 1984; Olsen, 1997).
Stebbins (1970) possivelmente já havia reconhecido o paradoxo, apontado
posteriormente por Ollerton (1996), quando propôs o Princípio do Polinizador Mais Efetivo
(Waser, 2006). Segundo Stebbins, sendo a seleção natural um processo quantitativo, a
adaptação floral ocorre mediante a interação com o polinizador mais freqüente e efetivo. Em
outras palavras, de todos os visitantes florais apenas aquele(s) mais efetivo(s) na transferência
do pólen e freqüente(s) na visita às flores vai(ão) exercer a força seletiva mais importante
(Fenster et al., 2004). Na concepção de Stebbins, portanto, estudar o sistema planta-
polinizador implica necessariamente na quantificação dos dois componentes da interação:
freqüência de visitas e eficácia na deposição de pólen sobre a superfície estigmática a cada
visita floral (Fenster et al., 2004).
Gómez e Zamora (2006) discutem que, para a seleção natural ocorrer, os polinizadores
devem favorecer a reprodução da planta devido à sua abundância nas flores e sua efetividade
na deposição de pólen, os componentes quantitativo e qualitativo da interação. Para que
ocorra especialização da planta em determinado polinizador, outra condição é a existência de
diferenças quanto à freqüência de visitas e transferência de pólen entre os demais visitantes.
Se diferentes visitantes apresentam a mesma eficácia na polinização, não há possibilidade de
especialização por parte da planta. Além disso, esses autores acrescentam que similaridade
entre diferentes polinizadores pode significar pouca variabilidade espaço-temporal na força
seletiva.
O Princípio do Polinizador Mais Efetivo enunciado por Stebbins, além de afirmar que
os polinizadores devem variar com relação à efetividade para que as plantas possam
desenvolver especialização, também assume que os componentes quantitativo e qualitativo da
efetividade do polinizador devam ser correlacionados positivamente já que a seleção natural
atuaria nos traços florais que atraem o polinizador mais eficiente ou mais abundante e
favoreceria a evolução de fenótipos que fizessem com que o polinizador mais abundante fosse
também o mais efetivo (Mayfield et al., 2001; Gómez e Zamora, 2006). Waser et al. (1996)
desenvolveram um modelo matemático que dá suporte a essa última suposição.
Apesar de muitos estudos terem confirmado a variação na efetividade do polinizador
entre diferentes visitantes florais, a esperada correlação positiva entre os componentes
quantitativo e qualitativo da interação não vem sendo observada com freqüência na natureza
(Mayfield et al., 2001; Gómez e Zamora, 2006).
Herrera (1987) afirma que a investigação dos componentes quantitativo e qualitativo
da interação é bastante relevante considerando que as interações planta-polinizador podem
promover forças seletivas mútuas e adaptação recíproca. Adicionalmente, Herrera (1989)
sugere que um modo de explorar o potencial evolutivo de um dado sistema planta-polinizador
é a investigação dos aspectos quantitativos e qualitativos e variação destes entre os
mutualistas (Schemske e Horvitz, 1984).
Herrera (1987) utilizou uma medida indireta da qualidade da polinização através dos
seguintes componentes: variação entre os visitantes quanto à freqüência de deposição de
pólen nos estigmas, número de grãos de pólen depositados e qualidade do pólen (viabilidade).
Diferenças no componente quantitativo foram baseadas na variação da abundância dos
visitantes e na taxa de visitação às flores (Herrera, 1989).
Herrera (1988) propõe que a investigação das diferenças entre visitantes florais quanto
aos componentes quantitativo e qualitativo da interação constitua um primeiro passo para
estudos posteriores acerca da variação espacial e temporal das interações planta-polinizador.
Fenster et al. (2004) relatam que os estudos utilizam uma variedade de métricas para
quantificar o aspecto qualitativo da interação, ou seja, a efetividade do polinizador na
transferência de pólen. Tais métricas incluem desde a taxa de deposição de pólen nos estigmas
para cada espécie de visitante, número de grãos de pólen depositados por visita, freqüência de
contato com anteras e estigmas de cada visitante, até a produção de frutos e sementes por
visita de cada espécie de visitante.
Spears (1983) afirma que para determinar a importância de cada visitante floral para
planta, é necessária a definição de uma medida da efetividade do polinizador. Existem várias
formas de se obter tal medida, sendo possível dividir entre medidas diretas e indiretas. As
medidas indiretas são baseadas em diversos componentes da qualidade da interação, como a
quantidade de pólen transferida para o estigma. Segundo o autor, tais medidas, apesar da
relativa facilidade na obtenção dos dados, são difíceis de serem analisadas estatisticamente.
Além disso, existe a dificuldade em relacionar diretamente as medidas à contribuição de cada
espécie de visitante para o sucesso reprodutivo da planta. Spears (1983) destaca ainda que a
contagem de grãos de pólen transferidos para o estigma não revela nada acerca da qualidade
daquele pólen ou sobre a produção bem sucedida de sementes a partir da flor em questão. Já
as medidas diretas da efetividade do polinizador provêm da produção de frutos e sementes por
uma população de plantas em resposta às visitas do polinizador e, por isso, necessitam de
muito menos suposições e trazem resultados mais claros do que as elaboradas medidas
indiretas.
Stone (1996) considera que a efetividade do polinizador é difícil de ser medida
diretamente, especialmente em sistemas com baixa taxa de visitação e que, por essa razão,
muitos estudos utilizam medidas indiretas. A autora destaca, no entanto, que integrar as
medidas indiretas em uma única medida do desempenho do polinizador representa um
problema adicional.
A maior parte dos estudos, porém, concentra a investigação no componente
quantitativo da interação já que a observação e quantificação da transferência de pólen
impõem maiores dificuldades (Herrera, 1987; Waser et al., 1996; Fenster et al., 2004).
Aigner (2006) afirma que a maioria dos estudos aborda apenas um aspecto do desempenho
dos polinizadores, sendo poucos os que abordam os componentes quantitativo e qualitativo no
mesmo sistema planta-polinizador. Na opinião deste autor, estudos que enfocam apenas um
dos componentes da interação podem apresentar parcialidade quanto aos seus resultados.
A caracterização dos aspectos quantitativos e qualitativos dos diferentes polinizadores
é essencial também na investigação acerca do gradiente especialização-generalização exibido
pelos sistemas planta-polinizador (Herrera, 2005; Sahli e Conner, 2006). Simples listas de
visitantes florais que uma planta recebe fornecem informação pouco útil para a questão de
especialização/generalização já que não há distinção entre visitantes e polinizadores efetivos.
Identificar os polinizadores dentre os visitantes florais representa um pré-requisito importante
em qualquer investigação de sistemas de polinização (Waser et al., 1996; Johnson e Steiner,
2000; Sahli e Conner, 2006).
Gómez (2000) e Gómez e Zamora (2006) salientam, no entanto, que considerar o
efeito dos polinizadores a partir de estimativas pré-dispersão, como quantidade de pólen
removido e depositado ou número de sementes produzidas por visita, representa uma primeira
aproximação acerca da efetividade dos mesmos sobre o sucesso reprodutivo da planta. É
importante que o efeito dos polinizadores seja também analisado em outros estágios do ciclo
de vida da planta, como por exemplo, na germinação (Herrera, 2000).
Aigner (2001) questiona a generalização do Princípio do Polinizador Mais Efetivo
(PPME) como um princípio organizador da evolução e ecologia floral, apesar de considerar
que as plantas podem frequentemente se especializar em seus polinizadores mais efetivos. Ao
contrário do PPME, o autor considera que a efetividade dos polinizadores não precisa ser
estreitamente relacionada com a importância destes como agentes de seleção porque as
plantas podem se especializar em polinizadores menos importantes quando esta adaptação não
compromete a interação com o polinizador mais comum e efetivo (Aigner, 2001; Mayfield et
al., 2001; Armbruster, 2006). Aigner (2001) e Armbruster (2006) afirmam, no entanto, que tal
hipótese ainda necessita ser testada empiricamente.
Gottsberger (1996) enfatiza que o estudo da biologia da polinização tem grande
potencial no teste de diversos paradigmas da biologia, como coevolução, mutualismo e
evolução, além da vital importância das interações planta-polinizador para a manutenção da
integridade estrutural e funcional dos ecossistemas naturais.
Bawa (1990) afirma que informação básica acerca da história natural das interações
planta-polinizador em florestas tropicais úmidas é limitada. Estudos empíricos são necessários
para determinar a especificidade dessas interações nesses ecossistemas de modo a gerar
informação importante sobre a estabilidade da comunidade, além de avaliar o grau de
coevolução entre as plantas e seus polinizadores. Apenas através de um entendimento mais
completo e quantitativo do papel que os animais desempenham como polinizadores em
diferentes ecossistemas é que pode haver uma noção mais clara acerca das implicações
ecológicas e evolutivas dessa importante interação mutualística (Waser, 2006).
Similarity in pollination effectiveness among the three floral visitors of Psychotria
brachybotrya (Rubiaceae) in the understory of primary forest in Central Amazonia,
Brazil.
Thaysa Nogueira de Moura
1
and Antonio Carlos Webber
2
.
1
Pós-graduação em Botânica nível mestrado, Instituto Nacional de Pesquisas da Amazônia.
2
Departamento de Biologia, Universidade Federal do Amazonas.
Running title: Similarity in pollination effectiveness
Corresponding author: Thaysa Nogueira de Moura ([email protected])
Adress:
INSTITUTO NACIONAL DE PESQUISAS DA AMAZÔNIA – INPA
Programa de Pós-graduação em Biologia Tropical e Recursos Naturais
Divisão do curso de pós-graduação em Botânica
Av. André Araújo, 2936 - Aleixo. Caixa Postal 478. CEP: 69060-001. Manaus/Amazonas -
Brazil.
Phone and fax number:
005592 36433119
Key words: Amazon Rainforest, frequency of visits, ecological generalization, plant-animal
interactions, Psychotria, understory.
ABSTRACT
In this paper we investigate the quality (per-visit effectiveness) and quantity (relative
abundance and frequency of visits) components of the interaction between a tropical distylous
shrub, Psychotria brachybotrya (Rubiaceae), and its floral visitor taxa. At the single
population studied in 2007, we registered three floral visitor species: Ceratina (Crewella) sp.,
Trigona fulviventris and Partamona sp., which had similar relative abundances and visitation
rates. The three bee taxa are effective pollinators of P. brachybotrya, a self and intra-morph
incompatible, non-apomitic species. To account for temporal and/or spatial variation in the
mutualist assemblage additional pollinator censuses were undertaken in 2008 at the
population previously investigated and in a second one 50 km distant from the former. All the
floral visitor taxa observed in 2007 were registered again in 2008 at both populations, with
Ceratina (Crewella) sp. and Trigona fulviventris responsible for the major proportion of
visits. Our results indicate that the similarity in the pollination ability among the floral
visitors limits the possibilities for P. brachybotrya to specialize on a particular pollination
agent. Contrary to the traditional expectations that heterostylous species depend on very
specialized pollination agents, our study reports that generalist flower visitors may also be
high quality pollination taxa.
INTRODUCTION
Specialization in plant-pollinator interactions has been considered for decades a common
outcome through evolutionary time (Waser et al., 1996, Waser 2006). The conventional
concept spread among evolutionary biologists is that plants frequently benefit from
specialization because of pollinator fidelity and pollination effectiveness, contributing to an
increase in pollen outcrossing (Johnson and Steiner 2000, Gomez and Zamora 2006). More
recently, a conflict between theory and empirical data has appointed some problems with the
traditional specialization notion, suggesting that generalized pollination systems may be far
more frequent in nature than imagined previously (Horvitz and Schemske 1990, Waser et al.,
1996, Johnson and Steiner 2000). Despite the existence of specialized adaptations of flowers
for particular pollinator agents, they are often visited by a diverse assemblage of species
(Herrera 1996, Ollerton 1996).
Many studies of plant-pollinator systems have reported variability on frequency of visits and
pollination effectiveness among the flower visitors that a plant receives (Herrera 1987, 1989;
Horvitz and Schemske 1990, Waser et al., 1996). Such variation offers an opportunity for a
plant to specialize on a particular pollinator agent (Herrera 1988, Horvitz and Schemske 1990,
Gomez and Zamora 2006). As highlighted by Herrera (1988), a crucial aspect in any
pollination investigation is the examination of differences among flower visitors in relation to
their effects on the fitness of the plant through their frequency of visits and pollination
effectiveness. However, if different flower visitors exhibit the same pollination ability, a
specialized interaction is constrained, which may also limit the spatio-temporal variability of
the selective force (Gomez and Zamora 2006).
The genus Psychotria L. is the largest one in the Rubiaceae with approximately 1650 species
(Nepokroef 1999) whose species are generally understory shrubs characterized by the small,
whitish flowers visited by a diverse assemblage of floral visitors such as bees, wasps,
butterflies, moths and hummingbirds (Castro and Oliveira 2002, Castro and Araujo 2004,
Nepokroef et al. 1999, Santos et al. 2008, Stone 1996, Teixeira e Machado 2004). Heterostyly
is the most common reproductive strategy found in this genus, being distyly considered a
primitive characteristic (Barrett and Richards 1990, Barrett 1992).
Heterostyly is thought to have evolved because it promotes outcrossing, reducing pollen
wastage through illegitimate pollination (Bjorkman 1995). A close reciprocal correspondence
between a heterostylous species flowers and particular pollinators is generally assumed to be a
critical aspect for successful pollination (Ganders 1979). But, Bjorkman (1995) argues that
effective pollination in heterostylous species may be unrelated to pollinator specialization.
In the present study we investigate the pollination system of Psychotria brachybotrya DC., an
understory distylous shrub of primary forest visited predominantly by three bee species. Our
field observations and experiments seek to examine per-visit effectiveness of the different
flower visitors taxa of P. brachybotrya, measured in terms of fruit set after single visit.
Besides, the frequency of visits and relative abundance of the floral visitors were analyzed
temporal and spatially.
STUDY SITE
The study was undertaken at the Fazenda Experimental da Universidade Federal do
Amazonas (2º 38’ 57,6”S 60º 3’ 11”W, 96 m altitude), located at km 38 of the federal road
BR-174, in Manaus, Amazonas, North Brazil. The study site has a hot, wet climate with
distinct rainy and dry seasons. The rainy season is from December to May and the dry season
from June to November. We marked 55 individual plants (28 pin and 27 thrum) of P.
brachybotrya in the understory of primary forest. The distance between individuals ranges
from 10-200 meters.
Additional pollinator censuses were conducted in 2008 at a second population in the Reserva
Florestal Adolpho Ducke located at km 28 of the state road AM-010, also in Manaus. We
marked six individual plants, being three pairs consisting of one pin and one thrum plant
along the trails at three plots distant one kilometer from each other.
METHODS
Data collection
Observations were carried out on the longevity of flowers and time of anthesis (20 flowers
from 20 individuals of each morph). Receptivity of the stigmatic area was determined by the
peroxidase technique (Kearns & Inouye 1993). We were not able to collect nectar due to the
reduced flower size and the insufficient volume of nectar for direct use of a refractometer.
The presence of scent-producing glands on flowers (osmophores) was tested with a neutral
red solution using 30 flowers from distinct individuals from each morph (Dafni 1992).
Floral morphometric data were collected for 20 flowers of each morph (20 individuals/morph)
where stigma and anther heights, stigma lobe, corolla length and diameter were recorded.
Data were recorded using a digital caliper (error, 0.01 mm) and a dissecting stereoscope.
Compatibility system was quantified comparing the fruit set resulting from the following hand
pollination experiments: self -, intramorph and intermorph pollinations and apomixis, using
one flower from 20 individuals from each morph (Castro and Araujo 2004). Flowers used in
the different treatments were color coded with a cotton thread near the pedicel and covered to
verify fruit set.
We conducted 15 pollinator censuses on 15 individuals (seven pin and eight thrum) at
Fazenda Experimental UFAM between 18 January and 2 March 2007, covering most part of
P. brachybotrya flowering season. After preliminary observations, we detected that most part
of visits were concentrated by the morning (0700h – 1200h). In order to standardize data for
statistical analysis, we defined a standard daily census period from 0700 to 1200h when
visitation is concentrated. During each census, we carefully watched the activity of flower
visitors at one marked treelet, recording the total number of flowers visited by each visitor
species. We then calculated the visitation rate for each visitor species dividing the total
number of flowers visited in each census by the total time of observation in each census (4
hours).We also calculated the relative abundance of each flower visitor as the number of visits
by the species divided by the total number of visits observed during the period of study
(Horvitz and Schemske 1990). To test per-visit effectiveness of the floral visitors, we exposed
unvisited, first day flowers to one visit of a single pollinator species. For these experiments,
we marked one flower on at least 17 plants (including pin and thrum individuals) which were
bagged after each census to verify fruit set. We recorded the number of buds and open flowers
of the marked treelets and quantified the fruit production of censused treelets in order to
obtain an indicator of pollination success under natural conditions. The flower visitors were
collected and identified by specialist.
To account for temporal and/or spatial variation in the pollinator assemblage, seven additional
censuses were conducted during the flowering peak in February 2008 at the previously
investigated population and other six censuses at a second population distant 50 km from the
former. For statistical analyses, we considered results significant if p ≤ 0.05.
RESULTS
Floral biology and breeding system
Psychotria brachybotrya flowered from January to March and each shrub displayed between
five and 15 flowers daily. Flowers are white, erect, tubular, sympetalous, synsepalous and
epigenous with a basal nectariferous disc inside the corolla. Androecium is isostemon with
epipetalous stamens. Gynoecium is syncarpic, consisting of a two-loculated and two-ovulated
ovary. Despite we could not perceive any floral scent, neutral red stained the corolla lobes
positively. Flowers of both morphs opened before 0700h and wilted at dusk. Pollen and nectar
were available in natural conditions since the beginning of anthesis until before 1100h.
The stigma and anther heights were statistically different between floral morphs indicating
that P. brachybotrya is a distylous species (Table 1). However, flowers are not exactly
reciprocal herkogamous, since we found that the stigma height of one morph was statistically
different to the anther height of the opposite morph (Table 1). Lobe and corolla lengths were
larger in thrum than in pin flowers, while corolla diameter was larger in pin flowers (Table 1).
In the breeding system experiments, fruit set only resulted after inter-morph (Pin: 5 fruits [20
flowers] Thrum: 7 fruits [20 flowers]) and control treatments (Pin: 6 fruits [20 flowers]
Thrum: 5 fruits [20 flowers]), indicating that P. brachybotrya is a self- and intra-morph
incompatible, non-apomitic species. All the produced fruits had full seed production (two
seeds per fruit).
Pollinator censuses
We registered three bee species along the censuses conducted in 2007: Trigona fulviventris,
Ceratina (Crewella) sp. and Partamona sp.. These three floral visitors foraged for both pollen
and nectar and started their visits from early in the morning (0700h). After 1000h, the visits
become rarer, at the same time when pollen was completely removed from the anthers.
In the pollination effectiveness experiment, all the bee taxa were considered effective
pollinators of P. brachybotrya (Table 2).
In relation to the quantity component of the interaction, relative abundance among the flower
visitor taxa was not significant different (Kruskal-Wallis ANOVA: 3.84, df = 2, P= 0.145).
We also did not find significant difference between the visitation rates among the pollinators
(Kruskal-Wallis ANOVA: 5.24, df = 2, P= 0.072).
Trigona fulviventris visited between 1 and 7.5 flowers per hour, corresponding to 30% of all
visits received by P. brachybotrya individual plants. Partamona sp. visited from 1.5 to 3
flowers/hour. It was responsible for 23% of all visits made by all floral visitors. And Ceratina
sp. performed 47% of visits, visiting between 0.5 and 4.75 flowers per hour. All flower
visitors visited both pin and thrum morphs indistinctly (Table 3). In 2007, Ceratina
(Crewella) sp. and Trigona fulviventris were registered throughout the most part of P.
brachybotrya flowering season, contrasting to Partamona sp. which was observed only
during the last five censuses covering the end of the flowering period (Table 3).
To account for a possible variation in the pollinator assemblage, we conducted additional
censuses (Table 4) during the peak of the flowering period in February 2008 at the previously
population studied (Site 1) and at another population (Site 2) distant 50 km from the former.
At Site 1, along the seven censuses (Table 4) on four thrum and three pin individual plants
(distant 10-500 m from each other), we registered Ceratina (Crewella) sp. (33% of all visits)
and Trigona fulviventris (40% of all visits). Besides, we observed two unidentified wasp and
butterfly species visiting flowers on the censused plants. At Site 2, during six censuses (Table
4) on three pin and three thrum individual plants (at three plots distant one km from each
other) we registered Ceratina (Crewella) sp. (38.5% of all visits), Trigona fulviventris (43.4%
of all visits) and Partamona sp. (4.8% of all visits). Other rarer flower visitors observed were
an unidentified butterfly species which visited flowers on only two plants.
DISCUSSION
Floral morphometric data and the breeding system treatments indicate that Psychotria
brachybotrya may be considered a self/intramorph incompatible, dimorphic species (distyly).
However, data collected at the two populations investigated also reveals the absence of
herkogamous flowers, characterized by the reciprocal positioning of the stigma and the
anthers (anthers and stigma at reciprocal heights). Besides, thrum parts such as stigma lobe
and corolla length were larger than in pin parts.
Self and intramorph incompatibility, isopletic populations (a 1:1 ratio in a population) and
reciprocal herkogamy are features commonly associated to typical distylous species (Ganders
1979). The lack of any of these features is interpreted as a case of atypical distyly (Castro and
Araujo 2004). The absence of reciprocal herkogamy was recorded in some tropical dimorphic
species of Psychotria (Castro and Araujo 2004, Faivre and MacDade 2001, Hamilton 1990).
Floral asymmetries, such as larger parts in thrum flowers, are commonly observed in
distylous species of Rubiaceae (Castro and Araujo 2004), and in other plant groups as well
(Ganders 1979). Although the larger thrum parts have been considered as a compensation for
the asymmetric pollen flow commonly observed on pin stigmas (Ganders 1979, Bjorkman
1995), asymmetries between floral morphs are not yet well understood.
There is a traditional notion that heterostyly represents a pollination mechanism where exists
a close reciprocal correspondence between the flower and pollinators and that, without
specialized floral visitors, successful pollination is limited (Bjorkman 1995, Herrera 1996).
Our results indicate that all flower visitors taxa are effective pollinators of P. brachybotrya.
However, this similarity in pollination effectiveness does not mean, necessarily, that these
pollinators are specialized. The tiny flowers of P. brachybotrya do not show any constraint on
the activity of flower visitor taxa, being pollen and nectar easily accessible.
The interaction between Trigona fulviventris and P. brachybotrya is a good example of the
lack of specificity of floral visitor taxa on this plant species. In many studies, T. fulviventris is
frequently considered a generalist nectar thief and an ineffective pollinator agent. Stone’
(1996) study on a tropical distylous shrub Psychotria suerrensis in Costa Rica did not
consider T. fulviventris an effective pollinator, despite its high visitation rates. But, a study on
Psychotria barbiflora in Northeastern Brazil considered T. fulviventris a legitimate pollinator
(Teixeira and Machado 2004). The contrasting behavior of this floral visitor taxon may be
interpreted as a consequence of the different flower size among the Psychotria spp. studied.
While in P. suerrensis the length of the corolla tube is on average 1.4 cm, in P. barbiflora and
P. brachybotrya flowers do not exceed 0.7 mm. Clearly, T. fulviventris, while foraging for
nectar and pollen, may only contact the floral reproductive organs in tiny flowers with no
morphological constraint to its activity.
An important aspect which may influence the pollination effectiveness similarity among
flower visitor taxa is that P. brachybotrya plants bear only two ovules per flower, meaning
that few pollen grains are required in fertilization (Johnson et al. 1995). Besides, instead of
visiting few isolated plants in a population, all the three floral visitor taxa were registered
visiting flowers of many plants across a considerable distance at both populations in the two
years investigated. This behavior, which constitutes the evenness of visitation, indicates that
the bee taxa are effective pollinators since, instead of returning to the flowers on a single
plant, they visit many plants in a population (Stone 1996). Other important feature of the bee
taxa’ behavior is that the time of visitation coincides with the time of the anther dehiscence in
P. brachybotrya, since the majority of their visits are performed early in the morning when
pollen is still available.
Despite the fact we did find an intra seasonal variation in the presence of one pollinator
(Partamona sp.) in 2007, its relative abundance was similar to the other two bee taxa. As we
conducted censuses during a short period of the flowering season in 2008, the contribution of
Partamona sp. to the relative abundance of P. brachybotrya pollinators could be
underestimated in our study.
In this system where the three flower visitor species show the same pollination ability, there is
still the possibility for specialization of P. brachybotrya on the most abundant pollinator
(Gomez and Zamora 2006). However, this seems to be unreasonable due to the relative
abundance similarity among flower visitor taxa detected in our study along the two years
investigated.
The three flower visitor species, being all effective pollination agents, are functional
equivalents from the plant species perspective (Gomez and Zamora 2006). This may indicate
that even if a spatiotemporal variation exists in the pollinator assemblage, the selection regime
faced by P. brachybotrya will be similar across locations and seasons (Gomez and Zamora
2006). In this scenario, evolutionary specialization is constrained by the similarity in the
relative abundance and pollination effectiveness among flower visitor taxa (Horvitz and
Schemske 1990, Waser et al. 1996).
AKNOWLEDGMENTS
We thank Marco Antonio de Freitas Mendonca, Sr. Laudelino, Sr. Deisivaldo and all the staff
of the Fazenda Experimental da Universidade Federal do Amazonas for essential logistical
support. Special thanks also to Marcio Oliveira (INPA) for kindly identifying the bees. This
study is part of the MSc. thesis of the first author (INPA/UFAM, CNPq grant).
REFERENCES
Barrett, S.C.H. and Richards, J.H. 1990. Heterostyly in tropical plants. Mem. New York Bot.
Grad., 55: 35-61.
Barrett, S.C.H. 1992. Heterostylous genetic polymorphisms: model systems for evolutionary
analysis. In: Barrett, S.C.H. (Eds.) Evolution and function of heterostyly. Springer. p. 1-29.
Bjorkman, T. 1995. The effectiveness of heterostyly in preventing illegitimate pollinations in
dish-shaped flowers. Sex Plant Reproduction, 8: 143-146.
Castro, C.C. and Oliveira, P.E. 2002. Pollination biology of distylous Rubiaceae in the
Atlantic rain forest, SE Brazil. Plant Biology, 4: 640-646.
Castro, C.C. and Araujo, A.C. 2004. Distyly and sequential pollinators of Psychotria nuda
(Rubiaceae) in the Atlantic rain forest, Brazil. Plant. Syst. Evol., 244: 131-139.
Dafni, A. 1992. Pollination ecology - a practical approach. Oxford University Press, Oxford.
Faivre, A.E. and McDade, L.A. 2001. Population-level variation in the expression of
heterostyly in three species of Rubiaceae: Does reciprocal placement of anthers and stigmas
characterize heterostyly? American Journal of Botany, 88(5): 841-853.
Ganders, F.R. 1979. The biology of heterostyly. N. Zeal. J. Bot., 17: 607-635.
Gómez, J.M. and Zamora, R. 2006. Ecological factors that promote the evolution of
generalization in pollination systems. In: Waser, N.M.; Ollerton, J. (Eds). Plant-pollinator
interactions – from specialization to generalization. The University of Chicago Press. p. 145-
166.
Hamilton, C.W. 1990. Variations on a distylous theme in a Mesoamerican Psychotria
subgenus Psychotria (Rubiaceae). Memoirs of the New York Botanical Garden, 55: 62-75.
Herrera, C.M. 1987. Components of pollinator “quality”: comparative analysis of a diverse
insect assemblage. Oikos, 50: 79-90.
Herrera, C.M. 1988. Variation in mutualisms: the spatio-temporal mosaic of a pollinator
assemblage. Biological Journal of the Linnean Society, 35: 95-125.
Herrera, C.M. 1989. Pollinator abundance, morphology, and flower visitation rate: analysis of
the “quantity” component in a plan-pollinator system. Oecologia, 80: 241-248.
Herrera, C.M. 1996. Floral traits and adaptation to insect pollination: a devil’s advocate
approach. Pp. 65-87 in Lloyd, D.G. & Barrett, S.C.H. (eds). Floral biology. Chapman and
Hall, New York.
Horvitz, C.C. and Schemske, D.W. 1990. Spatiotemporal variation in insect mutualists of a
Neotropical herb. Ecology, 71(3): 1085-1097.
Johnson, S.G.; Delph, L.F. and Elderkin, C.L. 1995. The effect of petal-size manipulation on
pollen removal, seed set, and insect-visitor behavior in Campanula americana. Oecologia,
102: 174-179.
Johnson, S.D. and Steiner, K.E. 2000. Generalization versus specialization in plant pollination
systems. Tree, 15(4): 140-143.
Kearns, C.A. and Inouye, D.W. 1993. Techniques for pollination biologists. University Press
Colorado, Niwot.
Mayfield, M.M.; Waser, N.M. and Price, M.V. 2001. Exploring the “Most Effective
Pollinator Principle” with complex flowers: bumblebees and Ipomopsis aggregata. Annals of
Botany, 88: 591-596.
Nepokroef, M.; Bremer. B. and Sytsma, K.J. 1999. Reorganization of the genus Psychotria
and tribe Psychotrieae (Rubiaceae) inferred from ITS and rbcL sequence data. Systematic
Botany, 24(1): 5-27.
Ollerton, J. 1996. Reconciling ecological processes with phylogenetic patterns: the apparent
paradox of plant-pollinator systems. Journal of Ecology, 84: 767-769.
Santos, O.A.; Webber, A.C. and Costa, F.R.C. 2008 Biologia reprodutiva de Psychotria
spectabilis Steyrm. e Palicourea cf. virens (Poepp. & Endl.) Standl. (Rubiaceae) em uma
floresta úmida na região de Manaus, AM, Brasil. Acta Botanica Brasilica, 22(1): 275-285.
Spears, E.E. 1983. A direct measure of pollinator effectiveness. Oecologia, 57: 196-199.
Stone, J.L. 1996. Components of pollination effectiveness in Psychotria surrensis, a tropical
distylous shrub. Oecologia, 107: 504-512.
Teixeira, L.A.G. and Machado, I.C. 2004. Biologia da polinizacao e sistema reprodutivo de
Psychotria barbiflora DC. (Rubiaceae). Acta Botanica Brasilica, 18(4): 853-862.
Waser, N.M; Chittka, L.; Price, M.V.; Williams, N.M. and Ollerton, J. 1996. Generalization
in pollination systems, and why it matters. Ecology, 77(4): 1043-1060.
Waser, N.M. 2006. Specialization and generalization in plant-pollinator interactions: a
historical perspective. In: Waser, N.M.; Ollerton, J. (Eds). Plant-pollinator interactions – from
specialization to generalization. The University of Chicago Press. p. 3-1
TABLE
Table 1. Mean ± SD values [mm] of floral traits (N = 20 flowers per morph) of Psychotria
brachybotrya in the Amazon rainforest, Brazil. T thrum flowers, P pin flowers, U Mann-
Whitney values.
1x4
U= 0 (P< 0.001);
2x3
U= 76 (P< 0.001).
Floral
Morph
Lobe length
a
Stigma
height
Anther
height
b
Corolla
length
Corolla
diameter
T
1.34 ± 0.10 3.12 ± 0.17
1
5.75 ± 0.35
2
5.11 ± 0.42 1.03 ± 0.10
P
1.05 ± 0.11 6.25 ± 0.66
3
4.45 ± 0.21
4
4.63 ± 0.40 1.09 ± 0.08
U
382 (P< 0.001) 0 (P< 0.001) 400 (P< 0.001) 67 (P< 0.001) 233 (P< 0.001)
a
1 stigma lobe/flower
b
1 anther/flower
TABLE
Table 2. Number of fruits resulted from the pollination effectiveness experiment of the three
floral visitors of Psychotria brachybotrya in Amazon rainforest, Brazil (number of
flowers/individuals used in parenthesis), P and T pin and thrum respectively. The produced
fruits had full seed production (two seeds per fruit).
Floral visitors P T
Trigona fulviventris
4 (9) 4 (9)
Ceratina sp. 4 (10) 6 (10)
Partamona sp. 4 (9) 3 (8)
Table 3. Visitation rates of the floral visitors of Psychotria brachybotrya in the Amazon rainforest, Brazil, registered along 15 censuses at
Fazenda Experimental UFAM (SITE 1) in 2007 (18
th
January – 2
th
March). Rates in bold represent the total number of visited flowers by each
pollinator species in each census divided by the total time of a census (4 hours). Total number of legitimate visits is represented in parenthesis
under each rate. P pin, T thrum. (NF) number of opened flowers per individual plant in each census.
Pollinator censuses 2007
Floral
visitors
1- P
(7 F)
2- T
(10 F)
3- P
(8 F)
4- P
(11 F)
5- T
(8 F)
6- T
(7 F)
7- P
(8 F)
8- T
(13 F)
9- T
(13 F)
10- P
(12 F)
11- P
(11 F)
12- T
(13 F)
13- P
(15 F)
14- T
(10 F)
15- T
(12 F)
Partamona
sp.
-
-
-
-
-
-
-
-
-
-
1.5
(3)
3
(8)
2.25
(7)
2.6
(15)
1.5
(3)
Ceratina sp.
-
-
-
-
2.75
(8)
4.75
(16)
1.75
(2)
1.75
(6)
0.5
(3)
4
(5)
3.25
(11)
0.5
(2)
2.75
(12)
0.5
(1)
3.75
(6)
Trigona
fulviventris
3
(4)
1
(2)
5.2
(9)
6.5
(10)
0.25
(2)
-
1.75
(3)
3.24
(5)
2.25
(2)
0.25
(1)
-
-
-
-
7.5
(8)
Table 4. Visitation rates of the floral visitors of Psychotria brachybotrya in the Amazon rainforest, Brazil, registered along seven censuses at
Fazenda Experimental UFAM – SITE 1 (10
th
-16
th
February) and five censuses at Reserva Florestal Adolpho Ducke – SITE 2 in 2008 (18
th
-22
th
February). Rates in bold represent the total number of visited flowers by each pollinator species in each census divided by the total time of a
census (4 hours). Total number of legitimate visits is represented in parenthesis under each rate. P pin, T thrum. (NF) number of opened flowers
per individual plant in each census.
Pollinator censuses 2008
Fazenda Experimental UFAM Reserva Florestal Adolpho Ducke
Floral
Visitors
1-P
(4 F)
2-T
(5 F)
3-P
(10 F)
4-P
(7 F)
5-T
(5 F)
6-P
(2 F)
7-T
(6 F)
1-P
(7 F)
2-T
(10 F)
3-T
(5 F)
4-T
(6 F)
5-P
(12 F)
Ceratina sp.
0.5
(1)
-
-
1.5
(3)
0.25
(1)
0.25
(4)
-
4.25
(7)
6.25
(9)
3.5
(6)
5.5
(10)
-
Partamona
sp.
-
-
-
-
-
-
-
-
-
0.25
(1)
0.25
(1)
1
(2)
Trigona
fulviventris
3.5
(3)
-
0.5
(2)
-
1.5
(2)
1.2
(1)
0.75
(3)
-
1
(1)
3.25
(6)
6
(12)
2.8
(17)
Unidentified
wasp
3
(4)
1
(2)
1.5
(1)
-
-
-
-
-
-
-
-
-
Unidentified
butterfly
-
-
-
-
-
0.5
(2)
0.5
(2)
-
-
2.75
(9)
1.25
(1)
Floral biology and pollinator effectiveness of the diurnal floral visitors of
Tabernaemontana undulata Vahl. (Apocynaceae) in the understory of Amazon Rainforest,
Brazil.
Running title: Pollinator effectiveness of the diurnal floral visitors of Tabernaemontana
undulata.
Key words: Amazon rainforest, Apocynaceae, pollinator effectiveness, Euglossine, plant-
pollinator interactions, Tabernaemontana.
Thaysa Nogueira de Moura
1
, Antonio Carlos Webber
2
& Liliane Noemia Torres de
Melo
1
1
INSTITUTO NACIONAL DE PESQUISAS DA AMAZONIA (INPA), Brazil.
2
UNIVERSIDADE FEDERAL DO AMAZONAS (UFAM), Brazil.
Postal address:
Thaysa Nogueira de Moura ([email protected])
INSTITUTO NACIONAL DE PESQUISAS DA AMAZÔNIA – INPA
Programa de Pós-graduação em Biologia Tropical e Recursos Naturais
Divisão do curso de pós-graduação em Botânica
Av. André Araújo, 2936 - Aleixo. Caixa Postal 478. CEP: 69060-001. Manaus/Amazonas -
Brazil.
ABSTRACT
In this paper we examined per-visit effectiveness, frequency of visits and relative abundance
of the diurnal floral visitor taxa of Tabernaemontana undulata (Apocynaceae) at two
populations located in the primary forest and in a disturbed area connected to the continuous
forest. In the pollinator censuses conducted in the primary forest population we registered
only Eulaema bombiformis. In the disturbed area, however, only Euglossa sp. was responsible
for visits on T. undulata flowers. E. bombiformis was not absent in the disturbed area, but
preferred to forage on pollen and nectar-rich flowers of two neighboring flowering species. In
the primary forest, T. undulata was the only treelet in flower in the end of the dry season. We
did not find significant differences regarding the frequency of visits and relative abundance
among the diurnal flower visitors at both sites. In the per-visit effectiveness experiment
among the bee species, we observed only one fruit produced after E. bombiformis’ visits.
More field observations are needed to a better understanding of the complex breeding system
of T. undulata and the pollen transference by the diurnal floral visitor taxa.
INTRODUCTION
There is a traditional notion that the evolution of floral diversity is based upon specialized
interactions of plant species and pollinators, which led to the classification of flowering plants
into pollination syndromes (Faegri e Pijl 1979). However, many studies realize that, even
plants that exhibit characteristics of one pollination syndrome may be visited by other
organisms which may contribute to their pollination on some level (Spears 1983, Waser et al.
1996). Otherwise, many of the organisms visiting a plant population may not be pollinating
agents, but nectar or pollen thieves that do not contribute to its reproduction (Spears 1983).
Ollerton (1996) pointed out an apparent paradox between the ecological processes and the
phylogenetic patterns, where many flowers exhibit specialization in floral traits, at the same
time that they receive a diverse range of flower visitors. One of the possible resolutions
proposed by Ollerton (1996) is that among all the flower visitors of a plant species only a
small proportion can effectively pollinate it. Differences in relation to pollination ability
among flower visitors are probably quite common in nature, but have been poorly studied
(Johnson and Steiner 2000, Ollerton 1996).
Simple lists of flower visitors received by a plant provide little useful information because
there is no distinction between visitors and effective pollinators. Identifying the pollen vectors
among the flower visitors represents an important requirement for any pollination system
investigation (Waser et al. 1996, Johnson and Steiner 2000, Sahli and Conner 2006).
The mainly tropical Apocynaceae s.s. is characterized by a complex pollination mechanism
favoring cross pollination. This may have evolved in order to attract insects with long and
strong mouth parts able to access the nectar in the tubular flowers (Darrault and Schlindwein
2005). Besides the complex floral morphology, the existence of secondary pollen presentation
co-occurring with herkogamy also indicates a specialized pollination mechanism in
Apocynaceae (Lopes and Machado 1999). The genus Tabernaemontana L. belongs to the
subfamily Rauvolfioideae in the Apocynaceae s.s. (Simoes et al. 2006) where information
regarding the breeding system and pollination biology are scarce. From the few registers on
pollination biology for the genus, there are two made in Central Brazil by Gottsberger and
Gottsberger (2006) for Tabernaemontana hystrix Steud. and T. solanifolia DC., both with
nocturnal flowers and classified as moth-pollinated by the authors.
Amazon Rainforest, the largest tropical forest in the world, harbors a striking richness of
animals and plants species (Whitmore 1998). Plant-animal systems, as all other kinds of
species interactions, are also a critical aspect of this biodiversity (Ollerton & Cranmer 2002,
Ollerton et al. 2006). Most plant species in this ecosystem, especially those from understory,
are dependent on biotic pollination (Janzen 1975). Nevertheless, basic data on pollination
biology are limited, probably as a consequence of the various logistical difficulties imposed
by the complex structure of tropical rainforests (Bawa 1990, Kay & Schemske 2003, Ollerton
et al. 2006).
To our knowledge there are no studies on Tabernaemontana undulata Vahl., an understory
treelet found in the Central Amazonia rainforest. Despite the fact that its flowers show
morphological features compatible to the moth-pollination syndrome, they are frequently
visited by Euglossine bees at the same time when they emit a strong sweet floral scent by the
morning. In this study we examine per-visit effectiveness, frequency of visits and relative
abundance of the diurnal floral visitors of T. undulata at two populations in Central
Amazonia. Our main question is: Do the diurnal floral visitors contribute to the pollination of
the moth-flowers of T. undulata?
STUDY SITE
The study was undertaken at the Fazenda Experimental da Universidade Federal do
Amazonas (2º 38’ 57,6”S 60º 3’ 11”W, 96 m altitude), located at km 38 of the federal road
BR-174, in Manaus, Amazonas, North Brazil. The Fazenda Experimental shows various
vegetation types, from which primary rainforest represents the largest portion of the total area.
The study site has a hot, wet climate with distinct rainy and dry seasons. The rainy season is
from December to May and the dry season from June to November.
We investigated two T. undulata populations at two different areas (Site 1 and Site 2) distant
from each other about two kilometers. Site 1 represents the primary, continuous forest where
ten individuals were marked. Site 2 is located in a secondary vegetation area where a
plantation of Brazilian nuts (Bertholletia excelsa) was made almost 40 years ago after
deforestation. The plantation was abandoned and the area is now re-connected to the
continuous forest, showing a mix of late successional and primary forest species. We also
marked ten individuals at Site 2. The distance between individuals in the two populations
ranges from 2-50 meters. We conducted additional observations at a third area (Site 3) in the
primary forest distant one kilometer from Site 1 and almost 500 meters from Site 2.
METHODS
Data collection
Observations were carried out on the morphology, size and longevity of flowers (11 flowers
from 10 individuals) and time of anthesis. Location of the stigmatic area of the style head was
determined by the peroxidase technique (Kearns & Inouye 1993). Five isolated flowers (five
individuals) were used to measure nectar volume, with a micro-syringe, and sugar
concentration, with a portable refractometer. Pollen viability was tested in 10 flowers (10
individuals) with acetocarmine (Radford et al. 1974). The number of ovules and pollen grains
was determined from 10 flowers. Compatibility system was tested by the fruit set resulting
from spontaneous self pollination (40 flowers from 20 individuals) and hand self pollination
(40 flowers from 20 individuals), following the methods described by Darrault & Schlindwein
(2005). Besides, 40 exposed flowers (20 individuals from the two populations) were marked
to verify fruit set under natural conditions.
We conducted pollinator censuses at Sites 1, 2 and 3 between 19 October and 14 November
2007, covering the total T. undulata flowering season. After preliminary observations, we
detected that most part of visits were concentrated by the morning (0900h – 1200h). We also
conducted nocturnal observations for two times, when no nocturnal flower visitors were
registered. In order to standardize data for statistical analysis, we defined a standard daily
census period from 0900 to 1200h when visitation is concentrated. We conducted 10 censuses
at Site 1 and other 10 at Site 2 in alternate days. At Site 3, four additional censuses were
undertaken along the flowering period. During each 3h-census, we carefully watched the
activity of flower visitors at one marked treelet, recording the total number of flowers visited
and the total time spent in flowers by each visitor species. We then calculated the visitation
rate as the average of number of flowers visited per census. To test the pollinator
effectiveness, we exposed unvisited, first day flowers to visits of a single pollinator species.
For these experiments, we marked two flowers per plant in both Sites 1 and 2 populations
(N=40) which were bagged after each census to verify posterior fruit set. Because of the low
visitation rates and, ultimately, of the short flowering period, we could conduct only one
census at each marked treelet in both populations. We recorded the number of buds and open
flowers of the marked treelets and quantified the fruit production of censused treelets at the
two populations in order to obtain an indicator of pollination success under natural conditions.
Most part of the visitation sequences were recorded with a video camera and flower visitors
were identified through these video observations. For statistical analyses, we considered
results significant if p ≤ 0.05.
RESULTS
Flower morphology, flower biology and compatibility system
Tabernaemontana undulata is a treelet which grows in the understory of terra firme forest.
Flowering occurs once in a year, in the end of the dry season from October to November. The
treelets produced between 45-78 floral buds and their inflorescences usually open four
flowers per day, following the steady state pattern described by Gentry (1974).
The flowers are hermaphrodite, salverform, presenting a long (mean= 29 mm; range= 24-33)
and narrow (mean diameter= 3.2 mm; range= 2.8-3.6) floral tube. The corolla tube is pale red-
white and the lobes are white flushed with red. The stamens are inserted on the corolla tube
and the sessile, introrse anthers form a cone around the apex of the style head, occupying the
entire inner part of the flower tube. The anthers shed their pollen grains onto the apex of the
style head, forming a pollen chamber characteristic of the tribe Tabernaemontaneae. The style
head shows three functional regions: (1) an apical, sterile region where pollen is deposited
(secondary pollen presentation), (2) a median region which produces a sticky substance, and
(3) a lower receptive region beneath a basal membranous ring. Upon contact with H
2
O
2
only
this lower region reacted by liberating oxygen.
The ovary is superior, containing 68 ovules on average (N=10; range= 59-74). The number of
pollen grains per flower was, on average, 3467 (N=10; range= 3030-3775). Pollen viability
was ca. 99%.
The flowers open around 0500h and last for one and a half day. Nectar is available only after
0800h. Mean nectar volume was 3μl. Sugar concentration varied from 16 to 23 percent. Only
first-day flowers have a sweet scent which is perceptible just at a very close distance.
However, after 0900h the floral fragrance intensified and we could perceive it ca. one meter
distant from the plant. The flower odor disappeared after 1800h.
In the compatibility system experiment, both hand and spontaneous self-pollination tests
resulted in a total failure of fruit production, suggesting that T. undulata is self-incompatible.
From the 40 exposed flowers (control), no one produced fruits under natural conditions.
Pollinator censuses
Site 1 – In the understory of the primary forest, T. undulata is one of the very few species
flowering in the end of the dry season. We found only two herbs species simultaneously
flowering: Heliconia sp. (Heliconiaceae), which was visited by hummingbirds and
Monotagma spicatum (Marantaceae) visited by an unidentified bee genus. In the 10 censuses
conducted, we registered only Eulaema bombiformis Packard (1869) visiting T. undulata
flowers at Site 1 (Figure 1). On average, E. bombiformis visited two times (Table 1) each
censused treelet and the interval between visits was 15-30 min. From the few E. bombiformis
visits received by a plant, most part is concentrated by the morning (0900-1200h), coinciding
with the time when nectar was fully available and the sweet floral odor intensified. After
1200h, E. bombiformis visited T. undulata flowers sporadically, but we never observed visits
after 1400h. After visiting all first-day flowers on the same plant, we often observed E.
bombiformis visiting other T. undulata plants in sequence. Despite we did not mark the bees,
we never saw two E. bombiformis individuals foraging simultaneously, which may indicate
that most part of visits were performed by a single bee individual.
Site 2 – This disturbed area now connected to the continuous forest has late successional
species growing together with some mature forest species. At the time of T. undulata
flowering season, two arboreal species were simultaneously flowering at Site 2: the late
successional species Bellucia cf. dichotoma (Melastomataceae), which was in the flowering
peak and the Brazilian nut Bertholletia excelsa (Lecythidaceae), starting its flowering period.
During all the 10 censuses, we registered Euglossa sp. dominating the visits to T. undulata
flowers (Figure 2). We also observed in just two censuses an unidentified butterfly species
visiting two flowers per individual. Along each 3h-census, we observed Euglossa sp.
performing a single visit on each censused treelet (Table 1), also visiting only first-day
flowers. Similar to E. bombiformis behavior at Site 1, Euglossa sp. concentrated its visits by
the morning (0900-1200h), with rare visits between 1200-1400h, which indicates that the
sweet floral fragrance plays an important role in T. undulata pollinators attraction. We
registered that, different from E. bombiformis at Site 1, Euglossa sp. frequently visited only
few opened flowers on the same plant and then moved to another T. undulata treelet. The fact
that we could not observe E. bombiformis visiting T. undulata flowers does not mean that this
bee species was absent at Site 2. By the contrary, before each census (0700-0900h), we could
observe E. bombiformis visiting frequently the pollen-rich flowers of Bellucia cf. dichotoma.
And despite we could not observe directly E. bombiformis visiting Bertholletia excelsa
because of the trees height (30 m), this is a serious possibility since the Brazilian nut species
represents an important nectar source for Euglossini bees and depends on them as its
pollinator agents.
Site 3 – In four additional censuses conducted in a primary forest area distant only 500 m
from Site 2, we registered only E. bombiformis at T. undulata flowers. The floral visitor
behavior was similar to that described for Site 1. In this area, we also found only Heliconia
sp. and Monotagma spicatum in flower.
Frequency of visits and pollination effectiveness
We did not find significant differences on visitation rates of E. bombiformis and Euglossa sp.
(Table 1) between the two populations at Sites 1 and 2 (Mann-Whitney U Test: 45, df = 1, P=
0.70). The number of visits performed by each pollinator taxa (Table 1) was not significant
different (Mann-Whitney U Test: 66, df = 1, P= 0.170), as well as the number of opened
flowers in the day when each treelet was censused (Table 1) in the two populations (Mann-
Whitney U Test: 48, df = 1, P= 0.877).
In the per-visit effectiveness test, from 20 marked flowers visited by E. bombiformis at Site 1
population, we registered only one fruit produced. At site 2, there was no fruit production.
Since T. undulata seems to be self-incompatible and, in fact, shows a whole complex
morphology preventing self-pollination, we consider that any fruit produced by a treelet must
be a consequence of the pollinators visits.
We quantified the number of buds and fruit production under natural conditions on each
censused treelet in both populations (Table 2). There was a higher fruit production (Table 1)
in Site 2 population compared to Site 1 (Mann-Whitney U Test: 15.5, df = 1, P= 0.008).
DISCUSSION
The arrangement of the flower parts in T. undulata represents a highly efficient pollination
mechanism, making autogamy difficult and favoring cross pollination. The floral structure
ensures that in a single visit the flower visitor first deposit outcross pollen on the stigmatic
surface and then transfers the self pollen. To self pollinate a flower, the flower visitor taxa
would have to visit the same flower at least twice in order to remove self pollen and then
deposit it onto the style head. However, we never observed E. bombiformis and Euglossa sp.
visiting a same flower consecutively.
Despite T. undulata pollination mechanism avoids self pollination, this does not prevent
geitonogamy. The pollinator effectiveness test failure may be explained by at least two
reasons: geitonogamy and a low fruit set pattern for this species. The deposition of self pollen
onto the stigma of a self-incompatible species may interfere with the growth of pollen tubes
from outcross pollination, resulting in a clogging effect. Observations of the foraging
behavior of the flower visitors indicated that E. bombiformis and Euglossa sp. visited all
opened flowers of the same treelet before move to another T. undulata individual.
Darrault & Schlindwein (2005) also considered that the best pollinator of Hancornia speciosa
(Apocynaceae) would visit only one or a few flowers of the same plant individual before
switch to flowers of another treelet, avoiding geitonogamy in this way. However, the clogging
effect through geitonogamy is unlikely to be the only reason for the very low fruit set
observed in the pollination effectiveness test and under natural conditions. Low levels of fruit
set are reported by a number of studies in Apocynaceae (Lopes & Machado 1999 and
references therein) which may represent a widespread feature for this family.
Euglossini bees are well-known for their trapline foraging on steady-state understory plants,
being considered important long flight distance pollinators (Borrell 2005, Endress 1994).
These bees show some flower constancy, visiting the same individual plants daily along their
feeding route (Janzen 1971). Flowers of species in Apocynaceae s.s. are considered important
nectar sources to Euglossine bees and, because they have long proboscides compatible to the
floral morphology commonly found in this plant family, these bees are generally considered
as pollinators (Tostes et al. 2003).
The salverform flowers of T. undulata show some features which allow a classification into
the moth-pollination syndrome such as flower color and presence of a narrow floral tube
(Endress 1994). In fact, the observed difference in fruit set between the two populations may
be related to visits from nocturnal pollinators. However, the fact that flowers are open by the
morning and that they emit an intense sweet floral scent, together with nectar availability at
this time, indicate that diurnal flower visitors, especially long-tongued ones, may contribute in
some level to T. undulata reproduction.
To test the per-visit effectiveness of the Euglossine bees we used a direct measure of
pollinator effectiveness by measuring the fruit set in response to pollinator visits, especially
because it requires fewer assumptions and supply clearer results (Spears 1983). Through this
method, we could observe that Eulaema bombiformis was able to transfer pollen and pollinate
one flower. This was not the case for Euglossa sp., which is interesting since the two bee
species have similar morphology and behavior. Due to the complex breeding system of T.
undulata, with very low fruit production even under natural conditions, an indirect measure of
pollinator effectiveness, such as the measure of the amount of pollen transferred to stigmas,
would be very important in a future stage of the present study in order to clarify the role of
these bee species as pollinators of T. undulata.
ACKOWLEDGEMENTS
We thank Marco Antonio and the staff of the Fazenda Experimental da Universidade Federal
do Amazonas for essential logistical support. This study is part of the MSc. thesis of the first
author (Instituto Nacional de Pesquisas da Amazonia, Brazil, CNPq grant).
LITERATURE CITED
BAWA, K.S. 1990. Plant-pollinator interactions in tropical rain forests. Annual Review of
Ecology and Systematics 21: 399-422.
BORRELL, B.J. 2005. Long tongues and loose niches: evolution of Euglossini bees and their
nectar flowers. Biotropica 37(4): 664-669.
DARRAULT, R.O. & SCHLINDWEIN, C. 2005. Limited fruit production in Hancornia
speciosa (Apocynaceae) and pollination by nocturnal and diurnal insects. Biotropica 37(3):
381-188.
DRESSLER, R.L. 1982. Biology of the orchid bees (Euglossini). Ann. Rev. Ecol. Syst. 13:
373-394.
ENDRESS, P.K. 1994. Diversity and evolutionary biology of tropical flowers. Cambridge
University Press, Cambridge. 511 pp.
FAEGRI, K.; Van Der PIJL, L. 1979. The principles of pollination ecology. Pergamon Press,
Oxford.
GENTRY, A.H. 1974. Flowering phenology and diversity in tropical Bignoniaceae.
Biotropica, 6: 64-68.
GOTTSBERGER, G. & GOTTSBERGER, I. 2006. Life in the cerrado: a South American
tropical seasonal vegetation. Vol. II. Pollination and seed dispersal. Reta Verlag, Ulm. 383
pp.
JANZEN, D.H. 1971. Euglossine bees as long distance pollinators of tropical plants. Science
171: 203-205.
JANZEN, D.H. 1975. Ecology of plants in the tropics. Arnold, London.
JOHNSON, S.D.; STEINER, K.E. 2000. Generalization versus specialization in plant
pollination systems. Tree, 15(4): 140-143.
KAY, K.M. & SCHEMSKE, D.W. 2003. Pollinator assemblages and visitation rates for 11
species of Neotropical Costus (Costaceae). Biotropica 35: 198-207.
KEARNS, C.A. & INOUYE, D.W. 1993. Techniques for pollination biologists. University
Press Colorado, Niwot.
LOPES, A. & MACHADO, I.C. 1999. Pollination and reproductive biology of Rauvoulfia
grandiflora (Apocynaceae): secondary pollen presentation, herkogamy and self-
incompatibility. Plant Biology 1: 547-553.
OLLERTON, J. 1996. Reconciling ecological processes with phylogenetic patterns: the
apparent paradox of plant-pollinator systems. Journal of Ecology, 84: 767-769.
OLLERTON, J. & CRANMER, L. 2002. Latitudinal trends in plant-pollinator interactions:
are tropical plants more specialized? Oikos 98: 340-350.
OLLERTON, J., JOHNSON, S.D. & HINGSTON, A.B. 2006. Geographical variation in
diversity and specificity of pollination systems. Pp. 283-308 in Waser, N.M. & Ollerton, J.
(eds). Plant-pollinator interactions: from specialization to generalization. Univ. Chicago
Press, Chicago. 445 pp.
OLLERTON, J., KILLICK, A., LAMBORN, E., WATTS, S. & WHISTON, M. 2007.
Multiple meanings and modes: on the many ways to be a generalist flower. Taxon 56:
RADFORD, A.E., DICKINSON, W.C., MASSEY, J.R. & BELL, C.R. 1974. Vascular plant
systematic. Harper & Row, New York.
SAHLI, H.F.; CONNER, J.K. 2006. Characterizing ecological generalization in plant-
pollination systems. Oecologia, 148: 365-372.
SIMOES, A.O.; LIVSHULTZ, T.; CONTI, E. & ENDRESS, M.E. 2006. Phylogeny and
systematics of the Rauvolfioideae (Apocynaceae) based molecular and morphological
evidence. Ann. Missouri Bot. Gard., 94: 268-297.
TOSTES, R.B.; VIEIRA, M.F. & CAMPOS, L.A.O. 2003. Polinizacao de Peltastes peltatus
(Vell.) Woodson (Apocynoideae, Apocynaceae) por abelhas euglossineas. Pp. 3-9 in Melo,
G.A.R. & Alves-dos-Santos, I. (eds). Apoidea Neotropica: Homenagem aos 90 anos de Jesus
Santiago Moure. Editora UNESC, Criciuma.
SPEARS, E.E. 1983. A direct measure of pollinator effectiveness. Oecologia, 57: 196-199.
WASER, N.M; CHITTKA, L.; PRICE, M.V.; WILLIAMS, N.M. & OLLERTON, J. 1996.
Generalization in pollination systems, and why it matters. Ecology 77(4): 1043-1060.
WHITMORE, T.C. 1998. An introduction to tropical rainforests (2nd edition). Oxford
University Press, Oxford.
Table 1.Visitation rates of the floral visitors of Tabernaemontana undulata in the Amazon rainforest, Brazil, registered along 20 censuses (Sites
1 and 2) at Fazenda Experimental UFAM in 2007 (19
th
October – 14
th
November). Rates in bold represent the total number of visited flowers by
each floral visitor species in each census divided by the total time of a census (3 hours). Total number of legitimate visits is represented in
parenthesis under each rate. (NF) number of opened flowers per individual plant in each census.
Pollinator censuses
Floral visitor SITE 1
1 (4F)
2 (2F) 3 (7F) 4 (3F) 5 (3F) 6 (2F) 7 (3F) 8 (2F) 9 (1F) 10 (5F)
Eulaema
bombiformis
2.6
(4)
0.6
(1)
2.3
(8)
1
(1)
1
(1)
0.6
(2)
1
(1)
- -
1
(3)
SITE 2
1(7F)
2 (3F) 3 (5F) 4 (4F) 5 (5F) 6 (2F) 7 (2F) 8 (2F) 9 (2F) 10 (2F)
Euglossa sp.
2.3
(1)
1
(1)
1.6
(1)
1.3
(1)
1.6
(1)
0.6
(1)
0.6
(1)
2.3
(1)
- -
TABLE
Table 2. The number of buds (NOF) on each censused treelet and number of fruits produced
under natural conditions by all censused plants in the two populations of Tabernaemontana
undulata in Central Amazonia. There are not significant differences in the number of buds
between the two populations (Mann-Whitney U Test: 35, df = 1, P= 0.256). The fruit set in
the two populations is significant different (Mann-Whitney U Test: 15.5, df = 1, P= 0.008).
SITE 1 SITE 2
Censused plants N. of Buds Fruit set N. of buds Fruit set
1 47 2 52 9
2 22 0 49 5
3 35 0 60 8
4 60 2 43 7
5 50 2 68 8
6 30 0 37 2
7 25 0 71 9
8 70 15 30 5
9 44 6 41 7
10 32 0 39 5
FIGURES
Figures 1 (left) and 2 (right): Eulaema bombiformis visiting Tabernaemontana undulata
flowers in the primary forest (Site 1) and Euglossa sp. foraging at flowers in a disturbed area
(Site 2).
CONCLUSÕES
Dados morfométricos florais indicam que Psychotria brachybotrya apresenta distilia, porém
suas flores não possuem hercogamia do tipo recíproca já que foi observado que a altura do
estigma de um morfo é estatisticamente diferente da altura da antera do morfo oposto. Os
experimentos do sistema reprodutivo indicam que a espécie é auto e intra-incompatível. Nos
censos dos polinizadores conduzidos na população da Fazenda Experimental UFAM em
2007, três espécies de abelhas foram consideradas polinizadores eficientes de P.
brachybotrya: Trigona fulviventris, Partamona sp. e Ceratina (Crewella) sp., as quais tiveram
taxas de visitação e abundância relativa similares. Em 2008, nos censos adicionais na
população previamente estudada e em uma segunda população distante 50 km da primeira, as
três espécies de abelhas foram novamente registradas, além de outros visitantes esporádicos.
A similaridade na efetividade da polinização, taxa de visitação e abundância relativa das três
espécies de abelhas limita a especialização de P. brachybotrya a seus agentes de polinização.
Consideramos que o sistema de polinização da espécie é ecologicamente generalista, onde há
mais de uma espécie de polinizador envolvida na interação.
Tabernaemontana undulata possui morfologia floral compatível com a síndrome de
polinização por mariposas, porém o fato das flores permanecerem receptivas de dia, ao
mesmo tempo em que néctar é ofertado e um intenso odor floral é emitido, sugere que
visitantes florais diurnos possam contribuir com a reprodução da espécie. Apenas foi possível
provar a efetividade na polinização para Eulaema bombiformis, não sendo possível comprovar
que Euglossa sp. também participe na polinização da espécie. Devido ao complexo sistema
reprodutivo de T. undulata, onde existe uma baixa taxa de produção de frutos mesmo em
condições naturais, o uso de método indireto para testar a efetividade do polinizador, como a
contagem do pólen depositado sobre o estigma, torna-se indispensável para o esclarecimento
do papel desempenhado pelas abelhas Euglossini na polinização da espécie.
REFERÊNCIAS BIBLIOGRÁFICAS
Aigner, P.A. 2001. Optimality modeling and fitness trade-offs: when should plants become
pollinator specialists? Oikos, 95(1): 177-184.
Aigner, P.A. 2006. The evolution of specialized floral phenotypes in a fine-grained
pollination environment. In: Waser, N.M.; Ollerton, J. (Eds). Plant-pollinator interactions –
from specialization to generalization. The University of Chicago Press. p. 23-46.
Armbruster, W.S. 2006. Evolutionary and ecological aspects of specialized pollination: views
from the Artic to the Tropics. In: Waser, N.M.; Ollerton, J. (Eds). Plant-pollinator
interactions – from specialization to generalization. The University of Chicago Press. p. 260-
282.
Barrett, S.C.H.; Richards, J.H. 1990. Heterostyly in tropical plants. Memoirs of the New York
Botanical Garden, 55: 35-61.
Barrett, S.C.H. 1992. Heterostylous genetic polymorphisms: model systems for evolutionary
analysis. In: Barrett, S.C.H. (Eds.) Evolution and function of heterostyly. Springer. p. 1-29.
Bawa, K.S. 1990. Plant-pollinator interactions in tropical rain forests. Annual Review of
Ecology and Systematics, 21: 399-422.
Bjorkman, T. 1995. The effectiveness of heterostyly in preventing illegitimate pollinations in
dish-shaped flowers. Sex Plant Reproduction, 8: 143-146.
Castro, C.C.; Oliveira, P.E. 2002. Pollination biology of distylous Rubiaceae in the Atlantic
rain forest, SE Brazil. Plant Biology, 4: 640-646.
Coelho, C.P.; Barbosa, A.A. 2003. Biologia reprodutiva de Palicourea macrobotrys Ruiz &
Pavon (Rubiaceae): um possível caso de homostilia no gênero Palicourea Aubl. Revista
Brasileira de Botânica, 26: 403-413.
Consolaro, H.; Silva, E.B.; Oliveira, P.E. 2005. Variação floral e biologia reprodutiva de
Manettia cordifolia Mart. (Rubiaceae). Revista Brasileira de Botânica, 28(1): 85-94.
Dafni, A. 1992. Pollination ecology - a practical approach. Oxford University Press, Oxford.
Darrault, R.O.; Schlindwein, C. 2005. Limited fruit production in Hancornia speciosa
(Apocynaceae) and pollination by nocturnal and diurnal insects. Biotropica, 37(3): 381-188.
Faegri, K.; Van Der Pijl, L. 1979. The principles of pollination ecology. Pergamon Press,
Oxford.
Fenster, C.B.; Armbruster, W.S.; Wilson, P.; Dudash, M.R.; Thomson, J.D. 2004. Pollination
syndromes and floral specialization. Annu. Rev. Ecol. Evol. Syst., 35: 375-403.
Gentry, A.H.; Emmons, L.H. 1987. Geographical variation in fertility, phenology, and
composition of the understory of Neotropical forests. Biotropica, 19(3): 216-227.
Gómez, J.M. 2000. Effectiveness of ants as pollinators of Lobularia maritima: effects on
main sequential fitness components of the host plant. Oecologia, 122: 90-97.
Gómez, J.M.; Zamora, R. 2006. Ecological factors that promote the evolution of
generalization in pollination systems. In: Waser, N.M.; Ollerton, J. (Eds). Plant-pollinator
interactions – from specialization to generalization. The University of Chicago Press. p. 145-
166.
Gottsberger, G. 1996. Floral ecology – Report on the years 1992 (1991) to 1994 (1995).
Progress in Botany, 57: 368-415.
Herrera, C.M. 1987. Components of pollinator “quality”: comparative analysis of a diverse
insect assemblage. Oikos, 50: 79-90.
Herrera, C.M. 1988. Variation in mutualisms: the spatio-temporal mosaic of a pollinator
assemblage. Biological Journal of the Linnean Society, 35: 95-125.
Herrera, C.M. 1989. Pollinator abundance, morphology, and flower visitation rate: analysis of
the “quantity” component in a plan-pollinator system. Oecologia, 80: 241-248.
Herrera, C.M. 1995. Microclimate and individual variation in pollinators: flowering plants are
more than their flowers. Ecology, 76(5): 1516-1524.
Herrera, C.M. 2000. Flower-to-seedling consequences of different pollination regimes in an
insect - pollinated shrub. Ecology, 81: 15- 29.
Johnson, S.D.; Steiner, K.E. 2000. Generalization versus specialization in plant pollination
systems. Tree, 15(4): 140-143.
Kearns, C.A.; Inouye, D.W. 1993. Techniques for pollination biologists. University Press
Colorado, Niwot.
Linhart, Y.B.; Feinsinger, P. 1980. Plant-hummingbird interactions: effects of island size and
degree of specialization on pollination. Journal of Ecology, 68: 745-760.
Lopes, A.; Machado, I.C. 1999. Pollination and reproductive biology of Rauvoulfia
grandiflora (Apocynaceae): secondary pollen presentation, herkogamy and self-
incompatibility. Plant Biology, 1: 547-553.
Mayfield, M.M.; Waser, N.M.; Price, M.V. 2001. Exploring the “Most Effective Pollinator
Principle” with complex flowers: bumblebees and Ipomopsis aggregata. Annals of Botany,
88: 591-596.
Ollerton, J. 1996. Reconciling ecological processes with phylogenetic patterns: the apparent
paradox of plant-pollinator systems. Journal of Ecology, 84: 767-769.
Olsen, K.M. 1997. Pollination effectiveness and pollinator importance in a population of
Heterotheca subaxillaris (Asteraceae). Oecologia, 109: 114-121.
Poulin, B.; Wright, S.J.; Lefebvre, G.; Calderón, O. 1999. Interspecific synchrony and
asynchrony in the fruiting phenologies of congeneric bird-dispersed plants in Panama.
Journal of Tropical Ecology, 15: 213-227.
Sahli, H.F.; Conner, J.K. 2006. Characterizing ecological generalization in plant-pollination
systems. Oecologia, 148: 365-372.
Schemske, D.W.; Horvitz, C.C. 1984. Variation among floral visitors in pollination ability: a
pre-condition for mutualism specialization. Science, 225: 519-521.
Snow, D.W.; Snow, B.K. 1986. Feeding ecology of hummingbirds in the Serra do Mar,
Southeastern Brazil. El Hornero, 12: 286-296.
Spears, E.E. 1983. A direct measure of pollinator effectiveness. Oecologia, 57: 196-199.
Stebbins, G.L. 1970. Adaptive radiation of reproductive characteristics in angiosperms, I:
Pollination mechanisms. Annual Review of Ecology and Systematics, 1: 307-326.
Stone, J.L. 1996. Components of pollination effectiveness in Psychotria surrensis, a tropical
distylous shrub. Oecologia, 107: 504-512.
Waser, N.M; Chittka, L.; Price, M.V.; Williams, N.M.; Ollerton, J. 1996. Generalization in
pollination systems, and why it matters. Ecology, 77(4): 1043-1060.
Waser, N.M. 2006. Specialization and generalization in plant-pollinator interactions: a
historical perspective. In: Waser, N.M.; Ollerton, J. (Eds). Plant-pollinator interactions –
from specialization to generalization. The University of Chicago Press. p. 3-17.
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