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Pollination biology in Jacaranda copaia (Aubl.) D. Don. (Bignoniaceae) at the “Floresta Nacional do Tapajós”, Central Amazon, Brazil

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Jacaranda copaia (Aubl.) D. Don is a pioneer tree widespread in the Brazilian Amazon, usually found colonizing forest gaps and altered areas, and the forest fragment edges. This study investigated aspects of the floral biology, breeding system and pollinators of J. copaia trees. Flowering lasts from August to November, during the low rainfall period extending up to four weeks per tree and 3-4 months for the population as a whole, characterizing a cornucopia flowering pattern. The fruit set ends in the beginning of the rainy season, with wind dispersed winged seeds. Fruit set from open pollination was 1.06% (n = 6,932). Hand pollination using self-pollen (n = 2,099) did not set fruits. Cross-pollination resulted in 6.54% fruit set (n = 2,524), representing six times more than the natural pollination rate (1.06%, n = 6,932). Flowers excluded from insect visitation (automatic self-pollination) did not set fruits (n = 5,372). Pollen tube growth down to ovary was detected under fluorescence microcoscopy in cross-pollinated and selfed pistils. The species is an obligate allogamous plant, with late-acting self-incompatibility system. Approximately 40 species of native bees visited the flowers, but the main pollinators were medium-sized solitary bees as Euglossa and Centris species due to the compatibility between their body sizes with the corolla tube, direct contact with the reproductive structures and high frequency of visits.
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Revista Brasil. Bot., V.31, n.3, p.517-527, jul.-set. 2008
Pollination biology in Jacaranda copaia (Aubl.) D. Don. (Bignoniaceae)
at the “Floresta Nacional do Tapajós”, Central Amazon, Brazil1
MÁRCIA MOTTA MAUÉS2,4, PAULO EUGÊNIO A. M. DE OLIVEIRA3 and
MILTON KANASHIRO2
(received: June 06, 2006; accepted: July 03, 2008)
ABSTRACT – (Pollination biology in Jacaranda copaia (Aubl.) D. Don (Bignoniaceae) at the “Floresta Nacional do
Tapajós”, Central Amazon, Brazil). Jacaranda copaia (Aubl.) D. Don is a pioneer tree widespread in the Brazilian Amazon,
usually found colonizing forest gaps and altered areas, and the forest fragment edges. This study investigated aspects of
the floral biology, breeding system and pollinators of J. copaia trees. Flowering lasts from August to November, during the
low rainfall period extending up to four weeks per tree and 3-4 months for the population as a whole, characterizing a
cornucopia flowering pattern. The fruit set ends in the beginning of the rainy season, with wind dispersed winged seeds.
Fruit set from open pollination was 1.06% (n = 6,932). Hand pollination using self-pollen (n = 2,099) did not set fruits.
Cross-pollination resulted in 6.54% fruit set (n = 2,524), representing six times more than the natural pollination rate
(1.06%, n = 6,932). Flowers excluded from insect visitation (automatic self-pollination) did not set fruits (n = 5,372).
Pollen tube growth down to ovary was detected under fluorescence microcoscopy in cross-pollinated and selfed pistils. The
species is an obligate allogamous plant, with late-acting self-incompatibility system. Approximately 40 species of native
bees visited the flowers, but the main pollinators were medium-sized solitary bees as Euglossa and Centris species due to
the compatibility between their body sizes with the corolla tube, direct contact with the reproductive structures and high
frequency of visits.
Key words - bees, floral biology, late-acting self-incompatibility (LSI), phenology, pollinators
RESUMO – (Biologia da polinização de Jacaranda copaia (Aubl.) D. Don (Bignoniaceae) na Floresta Nacional do Tapajós,
Amazônia Ocidental, Brasil). Jacaranda copaia (Aubl.) D. Don é uma árvore pioneira distribuída por toda Amazônia
brasileira, encontrada colonizando clareiras, áreas alteradas e bordas de fragmentos florestais. O presente estudo investigou
aspectos da biologia floral, sistema reprodutivo e polinizadores de J. copaia. O florescimento ocorre de agosto a novembro,
durante o período de menor precipitação pluviométrica, estendendo-se por até quatro semanas por indivíduo e três ou quatro
meses para a população, caracterizando um padrão de floração cornucopia. A frutificação termina no início da estação
chuvosa, com a dispersão anemocórica das sementes aladas. A taxa de frutificação natural foi de 1,06% (n = 6.932). As
flores autopolinizadas manualmente (n = 2.099) não produziram frutos. A polinização cruzada (n = 2.524) resultou em
6,54% frutos, representando seis vezes mais do que a polinização natural (1,06%, n = 6.932). As flores protegidas da visita
de polinizadores (autopolinização espontânea) não formaram frutos (n = 5.372). O crescimento dos tubos polínicos foi
detectado sob microscopia de fluorescência tanto nos pistilos autopolinizados quanto nos submetidos à polinização cruzada.
A espécie foi considerada alógama obrigatória, com mecanismo de auto-incompatibilidade de ação tardia. Aproximadamente
40 espécies de abelhas nativas visitaram as flores, entretanto os polinizadores legítimos foram principalmente abelhas
solitárias de médio porte dos gêneros Euglossa e Centris, em função da compatibilidade entre o tamanho corporal com o
tubo da corola, que facilitava o contato direto com as estruturas reprodutivas, e a elevada freqüência de visitas.
Palavras-chave - abelhas, auto-incompatibilidade de ação tardia, biologia floral, fenologia, polinizadores
Introduction
Large rainforest woody species are commonly self-
incompatible (Bawa 1974, 1990) and dependent on long
distance pollinators. But despite low density and sometimes
asynchronous flowering, which have led to misconceptions
about the ability of these plants to attract pollinators
and have allogamous fruit set (Corner 1954, Fedorov
1966), they do attract efficient long distance pollinators
as large solitary or subsocial bees (Bawa et al. 1985,
Dick et al. 2004). For the tropical Bignoniaceae, a diverse
assemblage of pollinators seems to have influenced
flowering morphology and guaranteed fruit-set of these
largely self-incompatible plants (Gentry 1974a, Gibbs
& Bianchi 1999, Bittencourt Júnior & Semir 2004,
Gottsberger & Silberbauer-Gottsberger 2006). Flowering
phenology patterns, defined according to the duration and
1. Part of PhD thesis developed at the Universidade de Brasília,
Departamento de Ecologia, Brasília, DF, Brazil.
2. Embrapa Amazônia Oriental, Laboratório de Entomologia, Caixa
Postal 48, 66017-970 Belém, PA, Brazil.
3. Universidade Federal de Uberlândia, Departamento de Biociências,
Caixa Postal 593, 38400-902 Uberlândia, MG, Brazil.
4. Corresponding author: marcia@cpatu.embrapa.br
M. M. Maués et al.: Pollination biology in Jacaranda copaia (Bignoniaceae)
518
intensity, were also related with pollination biology (Gentry
1974b, Van Schaik et al. 1993, Morellato et al. 2000).
Despite numerous studies on pollination biology of
the Bignoniaceae, few published studies have been
focused so far on Jacaranda species, e.g. J. macrantha
Cham. (Bittencourt 1981), J. caroba (Vell.) A. DC. (Vieira
et al. 1992) and J. racemosa Cham. (Bittencourt Júnior
& Semir 2006). These studies showed clear evidences
of self-incompatibility (SI) (Bittencourt 1981) and
ovarian or late-acting self-incompatibility (LSI) (Vieira
et al. 1992, Bittencourt Júnior & Semir 2006).
Gottsberger & Silberbauer-Gottsberger (2006) discuss
about the superimposed pollination system of this genus,
where three layered types of pollination coexist.
Jacaranda copaia (Aubl.) D. Don are medium to
large trees, up to 30-35 m tall and 75 cm of DBH under
natural conditions (Silva et al. 1985). It is a pioneer tree,
usually found colonizing forest gaps, altered areas, and
the edge of forest fragments (Guariguata et al. 1995).
The species can also be established inside the forest,
where adult trees can reach the canopy, despite being
more frequent at the understory (Ribeiro et al. 1999).
The species is distributed in the Neotropical region,
widespread in lowland moist and wet forest from Belize
to Bolivia, where two subspecies coexist (Gentry 1992),
J. copaia subspecies copaia and J. copaia subspecies
spectabilis, which are distinguished by features of the
leaves and fruits. However, the acceptance of these
subspecies is still controversial (Ribeiro et al. 1999,
Lohmann et al. 2006, Lohmann & Ulloa-Ulloa 2006).
J. copaia has been recommended for use in agroforestry,
reforestation and degraded land recovery projects in
South and Central America (Brienza Júnior et al. 1991),
but basic information on its reproductive biology in order
to subsidize its use was still lacking.
In this study, floral biology and breeding system
of J. copaia were investigated in Pará State, Brazil, in
order to provide information to future species use and
management. The species is one of the target species of
the Dendrogene project, coordinated by Embrapa
Amazônia Oriental and several partners. In this project,
some woody species with different ecological growing
conditions and life history strategies are being studied
for their genetic structure, reproductive process and
regeneration (Kanashiro et al. 2002).
Material and methods
The main study area was located at the “Floresta
Nacional doTapajós” (Flona Tapajós), in central Brazilian
Amazon (2.89° S and 54.95° W). It comprises approximately
600,000 hectares of lowland native forest which has been
submitted to controlled timber extraction and sustainable
forest management studies (Silva et al. 1985, Kanashiro et
al. 2002). The climate, according to Köppen classification,
is AmW, characterized by annual dry period of 2-3 months
and average rainfall of 2,000 mm (600 mm to 3,000 mm)
(Espírito-Santo et al. 2005). The average annual air temperature
is 25 °C, mean relative humidity is 86% (Carvalho et al.
2004). This forest may experience severe drought during El
Niño events (Nepstad et al. 2002). From 1999 to 2004, a
low impact selective logging project was conducted in 3,222
hectares under supervision of the “Instituto Brasileiro do
Meio Ambiente e Recursos Naturais Renováveis” (Ibama)
and the International Tropical Timber Organization (ITTO).
The study plot was a 500 ha area within this larger area
most of which is still untouched forest.
Complementary studies on floral biology and reproductive
systems were also done with adult trees (> 20 years) planted
at the experimental area of “Embrapa Amazônia Oriental”
in Belém, Pará State (1°27’ S and 48°29’ W). The climate
according to Köppen, is Afi, characterized by an average
annual temperature of 25.9 °C (21 °C to 31.6 °C) and annual
average rainfall of 2,900 mm.
Phenological observations were carried out every two
weeks from October 2001 to July 2004 on 60 Jacaranda
copaia trees, considering the occurrence, duration and
frequency of the following events: (1) flowering (e.g., floral
buds and flowers); (2) fruit set (e.g., immature fruit, mature
fruit and seed dispersal) and (3) leaf changes (e.g., juvenile
and mature leaf; partial and total defoliation), in accordance
with the methodology of Fournier & Charpantier (1975).
The phenological records were associated with meteorological
data (e.g., precipitation, temperature, relative humidity and
photoperiod) obtained in the same area from 2001 to 2003
by the LBA Project Team (2007), in accordance with Miller
et al. (2004).
Inflorescence structure, flower morphology and aspects
of the floral biology (anthesis, number of flowers opened/
day, flower longevity, stigma receptivity, pollen viability,
osmophores detection, sugar concentration and volume of
the nectar, pollen/ovule ratio), were observed in five trees
at Belém area, from August to October 2002. Peroxtesmo
KO (Dafni & Maués 1998) was used to check stigma
receptivity. The Peroxtesmo test indicates the main receptive
area on the stigma surface, which turns dark blue or purple
in contact with the solution. Pollen viability was tested with
the DAB procedure (Sigma Fast™ 3.3’ diaminobenzidine)
and in vitro pollen germination on sucrose and agar medium
(Dafni et al. 2005). The osmophores were detected with
neutral red solution (1:10,000; Kearns & Inouye 1993) in
fresh flowers. The flowers were immersed in the neutral
red solution for 30 minutes, removed and washed in distilled
water. Nectar was removed from previously bagged flowers
and volume estimated with 1 µL glass microcapillary tubes.
This procedure was carried out on fresh flowers (n = 30)
(two hours after fully opening) and other 30 flowers one
Revista Brasil. Bot., V.31, n.3, p.517-527, jul.-set. 2008 519
day after opening. Total sugar concentration or “sucrose
equivalents” on the nectar was scored after volume measurements
with a Bellingham & Stanley pocket refractometer (Dafni
et al. 2005). Different parts of the flower (corolla, calyx,
staminode, stamens, pistil) where placed in covered glass
vials for 5-10 minutes to organoleptic evaluation of scent
(Dafni et al. 2005).
Fresh flowers were collected and fixed on FAA (acetic
acid 5%, formaldehyde 5% and ethanol 90%) and 48 h later
transferred to ethanol 70% for laboratory analysis. The
floral morphology was described using stereomicroscope
and scanning electron microscope (SEM). Flower structure,
size, shape and color, as well as number of flowers per
inflorescence, number of opened flowers per day and flower
longevity were documented. Flower measurements were
carried out for fixed flowers in five plants. The number of
ovules and anthers were counted under stereomicroscope.
The number of pollen grains was estimated in three flowers
of each five plants, using all four anthers per flower, with a
haematocytometer. To estimate the number of pollen grains
per flower, each anther was gently squashed in 1 mL of 50%
ethanol + 0.5%-1% of detergent, to facilitate pollen removal
and homogeneous spread of pollen for counting under
microscope. Six sub samples of 1 µL where dropped on the
haemacytometer, counting all the pollen grains in a surface
unit (Dafni et al. 2005).
Hand pollination experiments in previously bagged
flowers were also performed to evaluate breeding system
using five different trees. The subsequent treatments were
carried out (following Radford et al. 1974): (1) cross-
pollination; (2) manual self-pollination; (3) spontaneous
(automatic) self-pollination; (4) control – tagged flowers
left to natural pollination. Fruits set from each treatment
were monitored until the complete fruit maturation, denoted
by the beginning of capsules’ dehiscence. In order to access
the pollen germination and pollen tube growth by means of
aniline blue staining and fluorescence microscopy (Martin
1959), 20 pistils of each treatment were collected 24 h and
48 h after manual pollination, fixed in FAA for 48 h and
preserved in ethanol 70%. The index of self-incompatibility
(ISI) was assessed by the ratio between fruit set from self-
and cross-pollinated pistils (Bullock 1985). The reproductive
efficacy (RE) was obtained by the ratio between fruit set of
natural and cross-pollinated pistils (Ruiz & Arroyo 1978).
In order to have access to tree crown and observe flower
visitors, a 34 m wood tower with a 2 m2 platform on its top
was built beside a target tree at the Tapajós forest site. Similar
platforms with 10-18 m were also built beside J. copaia
trees at the Embrapa site, to facilitate the handling of the
flowers throughout the controlled pollination experiments.
Observations of insect behavior on the flowers were
accomplished, as well as capture with insect nets and
photographic records, in order to identify legitimate
pollinators. Frequency of visits was considered as follows:
high (more than 20 visits per day), medium (at least 10 visits
per day) and low or occasional (less than five visits per day).
The observations were performed from 7:00 a.m. (anthesis
initiation) to 18:00 p.m. during five days (approximately
50 h). Most insects were identified by comparison with
previously identified specimens in the Entomological
collection of Embrapa Amazônia Oriental. The following
data about the insect visitors were registered: (1) species
name; (2) if there was any contact between the visitor body
and the reproductive structures of the flowers; (3) if pollen
or nectar was collected and/or consumed. These observations
were carried out during the main flowering season of 2001-
2002, from September to October, corresponding to
approximately 82 h of observations. Voucher specimens of
the studied plants, insect visitors and pollinators, were
deposited at the IAN Herbarium (numbers 178633, 176899,
176900, 17901, 17902) and the Entomological Museum of
the Embrapa Eastern Amazon.
Results
Jacaranda copaia displays large erect panicles up
to 37 cm long at the branches’ tip, with an average of
3,596 flowers (± 613, n = 9) per inflorescence and
96.4 ± 58 (n = 16) opened flowers per inflorescence per
day during the peak of the flowering phase. The total
blooming per inflorescence lasted an average of 35 days
(± 11, n = 5).
The most expressive flowering period occurred
during the dry season, extending from September to
December, when up to 97% of the individuals were
flowering (figure 1). The same pattern was found during
the whole study period, characterizing an annual flowering
pattern (sensu Newstrom et al. 1994). Fruit set occurred
from November to March, and the seed dispersal was
concentrated during the peak of the raining season, from
February to May. Leaf changes occurred just prior to
the flowering phase, mainly from June to August.
The flowers are hermaphrodite, zygomorphic and
nectariferous. The calyx is short (5-6 mm), cupular,
brown, glabrous and gamosepalous. The corolla is
tubular-infundibuliform, violet-blue (or lilac) in the outer
surface and white inside the petal hood (throat), pubescent,
gamopetalous, with five free lobes, 2.4-3.0 cm long.
Androecium presents four didynamous stamens and one
visually attractive staminode with glandular trichomes
and bifurcated apex. Anthers are basifixed and monothecate
(divaricate) with a mostly apical longitudinal opening,
which remains partially closed after the dehiscence,
without exposing totally the pollen grains (figure 2C
and 5). The gynoecium presents a single filiform style,
shorter than the staminode, with a bilobed tactile and
humid stigma covered with clavate papillae of distinct
lengths at the inner surface (figure 2A, 2E, 4, 5 and 6),
M. M. Maués et al.: Pollination biology in Jacaranda copaia (Bignoniaceae)
520
and a flattened and elongated ovary containing an
average of 243 (± 33, n = 20) ovules.
During pre-anthesis phase flower buds were closed
only by the petals edges, which opens with the simple
touch of the first visitor. The anthesis started from 7:30
to 8:30 a.m, according to visitors’ movement. The nectary
is a disk located at the base of the ovary. The anthers
dehisced soon after full anthesis phase, but the pollen
was released only when the visitors squeezed the anthers,
removing small amounts of pollen grains. The number
of pollen grains estimated per flower was 30,425 (n = 4),
and the pollen/ovule ratio was 125.2. The osmophores
were mainly located in the corolla and staminode, which
was consistent with results of the organoleptic test.
The best sucrose concentration for pollen germination
was 25%, in which case 70.8% of the pollen spread on
the agar media after 24 hours exhibited pollen tube growth.
The DAB test showed highest pollen viability period
among 8:00 to 9:00 a.m. (75.5%), decreasing gradually
during the rest of the day (figure 3). The nectar was
produced in small amounts during the flower life span.
The average volume in first day flowers was 1.01 µL
(± 0.2, n = 20; 0.5 to 1.5 µL) and for second day pistils
the volume was 1.06 µL (± 0.3, n = 32; 0.5 to 2 µL).
Sugar concentration varied from 23% to 41% (mean =
28.5% ± 4.4; n = 19) for first day flowers and from 20%
to 53 % (mean = 34.7% ± 6.7; n = 31) for second day
remaining pistils. Stigma receptivity is mainly located at
the inner surface (papillate) region, lasting from the anthesis
until 24 h of lifespan, as shown by the Peroxtesmo KO tests.
Flowers had a life span of approximately 24 h (intact
flower – holding all the verticiles), after which the corolla
Figure 1. Percentage of trees in flowering ( J), fruiting ( ) and seed dispersal ( ) of Jacaranda copaia at the “Floresta
Nacional do Tapajós”, Central Amazon region, from October 2001 to July 2004.
Figure 2. Jacaranda copaia flower. A. Opened flower
showing the reproductive organs and the staminode position
inside the corolla chamber. B. Pistil. C. Dehisced anther
with pollen grains. D. Flowers and flower buds. E. Staminode
with trichomes.
Revista Brasil. Bot., V.31, n.3, p.517-527, jul.-set. 2008 521
collapsed together with the stamens and staminode. The
calyx, nectary disc and pistil lasted for another day, and
nectar was still secreted, although very few visitors
collected nectar during this second day. Total abscission
of these flower structures occurred 48 h after flower
opening. The dry dehiscent fruits took approximately
four months to mature and comprised an average of 245
winged seeds (± 26, n = 25), which were wind dispersed.
There was a plethora of 61 different species of flower
visitors, including medium to large-sized bees, butterflies,
wasps and hummingbirds (table 1). Medium-sized bees
belonging to the genus Euglossa and Centris, were the
most frequent visitors in both study sites and the main
pollinators due to their frequency, body size and behavior.
These bees were usually the first visitors, assisting in
the process of anthesis, as they touched the petal lobes
triggering their final expansion and corolla opening. The
visits of Centris were very fast, lasting from 3 to 6 s
(n = 46). The euglossine bees were very frequent visitors
and their visits lasted 8 to 12 s (n = 55). The Centris
spp. entered the flower tube and collected both nectar
and pollen, pollen collection indicated by body grooming
after visits. As for Centris spp., Euglossa bees contacted
reproductive structures at every visit while entering the
corolla tube. When leaving the corolla chamber they
squeezed the anthers, receiving pollen on the upper head
and thorax. Their long glossa proved to be very useful
in nectar collection. Euglossa males were also frequent
visitors, but they were more restricted to the upper part
of the corolla chamber, where they grasped the inner
petal surface and, apparently the staminode trichomes
glands. Halictidae (Augochlora, Augochloropsis,
Pseudoaugochloropsis), Exomalopsis and Meliponina
(Paratetrapedia) used the staminode as a bridge to access
the nectary, and sometimes collected pollen adhered to
its trichomes, behaving as occasional pollinators.
The flower visitation period extended from 7:30 a.m.
to 17:00 p.m., with higher frequency of bees from 8:00 to
Figure 3. Pollen viability of Jacaranda copaia expressed in
percentage of stained pollen grains with DAB (Sigma Fast™
3.3’ diaminobenzidine).
Table 1. Flower visitors and pollinator agents collected in Jacaranda copaia at the “Floresta Nacional do Tapajós” (Tap)
and Belém (Bel), in the Brazilian Amazon. (O = occasional pollinator; L = legitimate pollinator; R = pollen/nectar robber;
+Floral resources used by the visitors/pollinators: P = pollen; N = nectar).
FLOWER VISITORS Locality Category Resource used+
INSECTA
HYMENOPTERA
Apidae
Aparatrigona impunctata (Ducke, 1986) Bel/Tap O P
Bombus brevivillus Franklin, 1913 Bel/Tap L N
Bombus transversalis (Olivier, 1789) Bel/Tap L N
Centris (Heterocentris) analis (Fabricius, 1804) Bel L N, P
Centris (Heterocentris) dichrootricha (Moure, 1945) Tap L N, P
Centris (Centris) flavifrons (Fabricius, 1775) Bel O N
Centris (Hemisiella) trigonoides Lepeletier, 1841 Bel/Tap L N, P
Centris sp. 1 Bel/Tap L N, P
Centris sp. 2 Bel/Tap L N, P
Epicharis (Epicharis) rustica (Olivier, 1789) Bel O N
Epicharis (Hoplepicharis) affinis Smith, 1874 Bel L N
Epicharis (Parepicharis) zonata Smith, 1854 Bel O N
Epicharis sp. 1 Tap O N
Eufriesea mussitans (Fabricius, 1787) Bel O N
Eufriesea surinamensis (Linnaeus, 1758) Bel O N
Eufriesea sp. Bel O N
continue
M. M. Maués et al.: Pollination biology in Jacaranda copaia (Bignoniaceae)
522
FLOWER VISITORS Locality Category Resource used+
Euglossa chlorina (Dressler, 1982) Bel L N, P
Euglossa sp. 1 Tap L N, P
Euglossa sp. 2 Tap L N, P
Euglossa sp. 3 Tap L N, P
Euglossa sp. 4 Tap L N, P
Eulaema meriana (Olivier, 1789) Bel O N
Eulaema nigrita Lepeletier, 1841 Bel L N
Exomalopsis sp. 1 Bel O P
Exomalopsis sp. 2 Bel O P
Melipona compressipes (Fabricius, 1804) Tap O N, P
Meliponina (6 species) Tap O P
Paratetrapedia sp. 1 Bel O P
Paratetrapedia sp. 2 Bel O P
Xylocopa frontalis (Olivier, 1789) Bel R N
Megachilidae
Megachile (Chrysosaurus) ruficornis Smith, 1853 Tap O N
Andrenidae
Oxaea sp. Tap O N
Halictidae
Augochlora (Augochlora) esox (Vachall, 1911) Bel O N
Ceratina sp. 1 Tap O N
Pseudoaugochlora sp. 1 Bel O N, P
Pseudoaugochlora sp. 2 Tap O N, P
Vespidae
Synoeca virginea (Fabricius, 1804) Bel/Tap O N
DIPTERA
Bibionidae
1 species Tap O P
Syrphidae
Ornidia obesa Fabricius, 1775 Bel O P
COLEOPTERA
Chrysomelidae
4 species Tap O P
Scarabaeidade
Cnemida leprieuri Arrow 1899 Tap O P
Cnemida retusa (Fabricius, 1801) Tap O P
Scarabaeinae (2 species) Tap O P
LEPIDOPTERA
Pieridae
Phoebis statira (Cramer, 1777) Bel/Tap R N
Phoebis trite (Linnaeus, 1758) Tap R N
Lycaenidae
1 species Tap O N
Nymphalidae
Philaetria dido (Linnaeus, 1763) Tap O N
AVES
Trochilidae
Anthracothorax nigricollis (Vieillot, 1817) Bel/Tap O N
Glaucis hirsuta Gmelin (1788) Tap O N
Hylocharis sapphirina Gmelin (1788) Tap O N
Thalurania furcata (Gmelin, 1788) Bel O N
Topaza pella (Linnaeus, 1758) Tap O N
continuation
Revista Brasil. Bot., V.31, n.3, p.517-527, jul.-set. 2008 523
10:30 a.m. Xylocopa frontalis visited the flowers at irregular
intervals from the beginning of anthesis to the end of the
day, perforating the base of the corolla tube to take the
nectar in illegitimate visits which resulted in no pollination.
Butterflies were late visitors, from 11:00 a.m. to 15:30 p.m.,
and nectar robbers, using the holes made by X. frontalis
to access the nectar chamber. The legitimate and illegitimate
pollinators visited the flowers together along the day,
although the illegitimate visitors (e.g. Xylocopa and
butterflies) were more frequent during the afternoon. No
aggressive behavior was noticed among them.
Controlled pollination tests (table 2) resulted in no
fruit set from manual and automaticself-pollination,
although a single selfed fruit was initiated and aborted
two weeks after manual pollination. Fruit set from open
pollination was initially 4.99% but only 1.06% reached
maturation (n = 6,932). Cross-pollination resulted in
21.7% of initiated fruits but only 6.54% reached maturation
(n = 2,524). Pollen tube growth was detected both in
self and cross-pollinated pistils after the first 24 hours,
but only cross-pollen penetrated the ovules (figure 7).
Figures 4-7. Scanning electron micrography (SEM) of Jacaranda copaia flower. 4. Staminode apical region (38x). 5. Dehisced
anther (33x). 6. Stigmatic lobes (48x). 7. Pollen tubes penetrating the ovules 48 hours after cross-pollination under epifluorescence
pistil.
Table 2. Percentage (%) of fruit set from hand-pollination
treatments and open pollination flowers (control) in
Jacaranda copaia. Data corresponds to initiated (three
weeks) and mature fruits (number of fruits/number of flowers
per treatment). (ISI = Self-incompatibility index; RE =
Reproductive efficacy).
Treatments Initiated Mature
fruits fruits
Cross-pollination 21.7% 6.54%
(469/2,524) (173/2,524)
Manual self-pollination 0.06% 0
(1/2,099) (0/2,099)
Automatic self-pollination 0 0
(0/5,372) (0/5,372)
Control (open pollination) 4.99% 1.06%
(414/6,932) (91/6,932)
ISI 0
RE 0.16
45
67
M. M. Maués et al.: Pollination biology in Jacaranda copaia (Bignoniaceae)
524
Discussion
Jacaranda copaia flowers attributes, such as diurnal
anthesis, tubular violet zygomorphic corolla, presence
of nectar in a protected chamber, hidden reproductive
organs and sweet fragrance are compatible with the bee
pollination syndrome (Faegri & van der Pijl 1979, Proctor
et al. 1996). According to Gentry’s (1974a) classification,
Jacaranda copaia flowers belong to the Anemopaegma
type, generally pollinated by medium to large bees, usually
Euglossini and Anthophorinae, although it may be visited
by illegitimate pollinators, nectar and pollen robbers (e.g.
Trochlidae, Meliponina, Lepidoptera and Xylocopa). The
anther’s monothecate type is atypical within the genus
Jacaranda, as most species presents dithecate anthers
(Dr. Lúcia Lohmann, unpublished data).
The flowering phenology of Jacaranda copaia can
be classified as cornucopia (Gentry 1974b) with a relatively
long and massive flowering period between 3 to 10
weeks. The large and showy inflorescences at the canopy
layer, with hundreds of flowers opening at the flowering
peak, results in a flowering display which may attract
visitors from long distances. This flowering pattern
seems to be the most widespread and generalized among
the Bignoniaceae (Gentry 1974a)
The corolla tube allowed visits of small to medium-
sized bees and was a constraint to larger visitors. The
position of the anthers and stigma inside the petal hood
promoted the pollen deposition on the upper head and
thorax of the pollinators. The basal constriction of the
corolla tube was compatible with long-tongued bees, such
as Euglossa, as reported also by Bittencourt Júnior &
Semir (2006). The same foraging behavior of these agents
was registered in the pollination biology of Arrabidaea
conjugata (Vell.) Mart. (Correia et al. 2005) and Jacaranda
racemosa Cham. (Bittencourt Júnior & Semir 2006).
Euglossini female bees were considered the most
efficient melittophilous pollinators of Bignoniaceae
species in Panama (Gentry 1974b). The characteristic
long glossa of this tribe helps in the process of nectar
foraging in tubular flowers (Pinheiro & Schlindwein
1998). Centris were also reported as main pollinators
of Tabebuia flowers in Costa Rica (Frankie et al. 1983)
and Central Brazil (Barros 2001). Besides, Centris spp.
bees also demonstrated compatible pollinator behavior,
once they penetrated up to the second third of the corolla
tube (distal part), where the anthers and stigma are
located, and thus were able to properly transfer pollen
to the reproductive structures.
On the other hand, some of the visitors, as Xylocopa
frontalis, which were not able to enter the corolla tube,
collected nectar by perforating the soft corolla tissue at
the nectary level. This behavior has been recognized in
many species of the Bignoniaceae family (Gentry 1974a,
b, Gobatto-Rodrigues & Stort 1992, Vieira et al. 1992,
Galetto 1995, Correia et al. 2005) and is repeated by
Xylocopa bees in other plants with tubular flowers
(Barrows 1980).
The staminode “selected” the legitimate visits
reducing the corolla chamber, therefore large-sized visitors
were not able to properly enter the flower and contact
the stigma and anthers, although some species such as
Centris flavifrons, C. similes, Eulaema meriana, Epicharis
rustica, Bombus, Eufriesea and Oxaea forced the entrance
and acted as occasional pollinators, usually collecting
nectar. It was also used as a platform by smaller bees
such as Meliponina, Halictidae and Exomalopsis, which
used the staminode as a path to reach the nectar chamber.
The staminode function has been comprehensively
discussed (Bittencourt Júnior & Semir 2006, Gottsberger
& Silberbauer-Gottsberger 2006). Vieira et al. (1992)
suggested that this structure had three different functions
in Jacaranda caroba (Vell.) DC. flowers: visual
orientation, smell attraction guide and assistance in the
contact of the pollinators with the reproductive structures.
It has been also suggested that the staminode may be
used as a bridge by halictid bees to reach the anthers,
eventually touching the stigma (Gottsberger & Silberbauer-
Gottsberger 2006). It also retains pollen grains on the
glandular hairs (trichomes), which are collected by bees
(Morawetz 1982 apud Gottsberger & Silberbauer-
Gottsberger 2006), and diminishes the space inside the
corolla chamber, thus promoting better contact of the
pollinators with the reproductive organs (Bittencourt
Júnior & Semir 2006). In J. copaia, all those functions
can be assumed.
Finally, staminode’s trichomes secret a scent
(Bittencourt Júnior & Semir 2006) which may explain
the visits of Euglossa males. Due to those different
attractants, including nectar, pollen and scent, besides
the multiple role of the staminode adapting the flower to
different sizes of visitors, Jacaranda seems to have
superimposed pollination systems (Gottsberger &
Silberbauer-Gottsberger 2006).
Jacaranda copaia is self-incompatible with
abscission of selfed pistils within one or two days after
hand pollinations. ISI was null and the reproductive
efficacy 0.16 was very low, indicating that natural
pollination in the Belém plantation is much less efficient
than hand cross pollination. Pollen germination and pollen
tube growth was similar in both self and cross-pollinated
pistils, but in selfed pistils the pollen tubes were not
Revista Brasil. Bot., V.31, n.3, p.517-527, jul.-set. 2008 525
observed penetrating the ovules. This type of late-acting
self-incompatibility system (LSI) or ovarian self-
incompatibility (Seavey & Bawa 1986) is common in
many tropical Bignoniaceae, including Tabebuia aurea
(Manso) Benth. & Hook. f. ex S. Moore (syn. T. caraiba)
and T. ochracea (Cham.) Standl. (Gibbs & Bianchi 1993,
Barros 2001), Dolichandra cynanchoides Cham. and
Tabebuia nodosa (Griseb.) Griseb. (Gibbs & Bianchi,
1999), Jacaranda macrantha (Bittencourt 1981) and
Jacaranda racemosa (Bittencourt Júnior & Semir 2006).
Studies over the last two decades have shown that
outbreeding and LSI are common features in many
tropical trees (Bawa et al., 1985) but seem to be such
common features in the Bignoniaceae that a phylogenetic
component has been argued to explain such familial
clustering (Gibbs & Bianchi 1999). However, self-
fertility and apomixis have been also described in some
woody tropical Bignoniaceae (Costa et al. 2004). The
extremely low fruit set from open pollination is consistent
with other tropical trees (Bawa et al. 1985).
The pollen/ovule ration sensu Cruden (1977) indicated
that the species would be self-compatible, but field tests
on the reproductive system refuted that supposition. The
pollen grains are not exposed, but released from the anthers
in small amounts according to pollinators’ movements
in the flowers. This may result in a very efficient pollen
dispensing and pollination strategy, which may explain
the relatively low number of pollen grains produced per
flower. In Arrabidaea conjugata the pollen was released
by the same process, therefore even when visitors arrived
at the end of the anthesis they still can be dusted with
pollen grains (Correia et al. 2005).
The legitimate visitors observed confirmed the
melittophilous pollination syndrome sensu Faegri & van
der Pjil (1979) in J. copaia. Solitary bees tend to show
higher oligolectic species-specific preferences (Cane
2001), but the superimposed pollination system (Gottsberger
& Silberbauer-Gottsberger 2006), with nectar, pollen
and perfume as rewards, would explain the great number
of potential pollinators attracted. Hummingbird pollination
is reported in Zeyheria montana. Mart. (Bittencourt Júnior
& Semir 2004), but in J. copaia these agents were
considered simply occasional pollinators, due to their low
frequency and unspecialized bird syndrome flower traits.
Cornucopia flowering phenology also contributes to long
distance pollinators’ attraction. Roubik & Degen (2004)
modelling studies with J. copaia trees at the “Floresta
Nacional do Tapajós”, showed that this species was nearly
completely out-crosser and the mean pollen dispersal
range was 147.9 (± 42.0 m). Assuming that in this site the
species is regularly distributed (1.8 trees ³ 20 cm DBH
per hectare), and considering its diversified pollination
system, we expect the maintenance of the reproductive
success of J. copaia under natural conditions.
Acknowledgements – The authors are grateful to the
Dendrogene team, to the Department for International
Development (DFID) and Embrapa for their support during
all the study phases. To the “Floresta Nacional do Tapajós”
Administration (Ibama), for the permission to work at the
study site. To Lyn Loveless (College of Wooster, Ohio, USA)
and David Boshier (Oxford Forestry Institute, UK), for
valuable discussions and guidance. We also thank Antônio
Elielson Rocha from the Museu Paraense Emílio Goeldi, who
prepared the flower illustration; Francisco G. da Silva Frota,
Domingos de Jesus Araújo, Marco Antônio Cordeiro and
Reginaldo Medeiros (Entomology lab, Embrapa Amazônia
Oriental) along with Milene Souza, Fernando Santos and
Gleicilene Almeida (Universidade Federal Rural da Amazônia)
who assisted in field and lab work; Dr. David W. Roubik
(Smithsonian Tropical Research Institute) and Dr. Fernando
Silveira (Universidade Federal de Minas Gerais), who assisted
with the bees’ identification; two anonymous reviewers who
helped to improve the manuscript and, last but not least,
the field staff of the Dendrogene Project for all the effort
during data collection and assistance inside the project area.
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... Exine sculpture in pollen of a lot of genera of Bignoniaceae is reticulate (Burelo-Ramos et al. 2009). All species in this family are zoophilous (Gentry 1974), with bees being the major pollinators (Gentry 1974;Galetto 1995), so that in Jacaranda copaia, approximately 40 species of native bees visited the flowers (Maués et al. 2008). Pollination by birds, bats, hawk moths and butterflies also occurs (Weber and Vogel 1986;Gentry 1990;Lohmann 2002;Lopes et al. 2002), with one known occurrence of pollination by lemurs in Madagascar (Zjhra 2006). ...
... Cytomixis is more prevalent in genetically, physiologically and biochemically imbalanced plants such as triploids, haploids, hybrids, aneuploids, apomicts and polyploids (Nirmala and Rao 1996;Singhal et al. 2007). There are also reports of occurrence low fertility, seedlessnes, apomixes, polyploidy and asexual reproduction in family Bignoniaceae (Chauhan et al. 1987;Gibbs and Bianchi 1999;Barros 2001;Lopes et al. 2002;Maués et al. 2008;Firetti-Leggiere et al. 2011Gunaga et al. 2012a, b;Alves et al. 2013). Thus, the most likely explanation for the cause of seedless Fig. 9 SEM micrographs of pollen structure in T. undulata. ...
... Observations show that all species in this family are zoophilous (Gentry 1974), with bees being the major pollinators (Gentry 1974;Endress 1994;Galetto 1995;Maués et al. 2008). Pollination by birds, bats, hawkmoths, butterflies and one known occurrence of pollination by lemurs in Madagascar has also observed (Weber and Vogel 1986;Zjhra 2006;Gentry 1990;Lohmann 2002;Lopes et al. 2002). ...
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The genus Jacaranda shows notable karyotype stability and a prevailing self-sterile breeding system with evidence of late-acting selfincompatibility in several species. However, some studies have indicated self-compatibility in J. mimosifolia, a species cultivated worldwide in tropical and subtropical areas. Jacaranda cuspidifolia is a close related species with natural distribution broadly overlapping to that of J. mimosifolia, and manual heterospecific pollination studies have indicated that these species are interfertile, but there is no report on the breeding system of the former. In this study, we used hand-pollination experiments, pistil longevity, epi-fluorescence and histological analysis of post-pollination events to determine the breeding system of J. cuspidifolia. We also employed intra and interspecific crosses and seed germination tests to reevaluate the breeding system in J. mimosifolia and the inter-fertility between the two species. Some fruits were initiated from self-pollinated pistils in J. mimosifolia, but none of them reached maturity. On the other hand, complete absence of fruit development by self-pollination was verified in J. cuspidifolia, while in situ pollen tube growth and histological analysis of post-pollination events in selfed pistils revealed the characteristic ovule penetration, fertilization and endosperm initiation, as observed in other bignoniaceous species with late-acting self-incompatibility. Low outbreeding barriers seem to operate between these species because reciprocal interspecific crosses and hybrid seed germination tests indicated they are bilaterally interfertile. However, fruit/seed production and seed germinability were significantly lower when pistils of J. cuspidifolia were pollinated with pollen of J. mimosifolia, compared with crosses in the opposite direction, which indicates a partial unilateral incompatibility. This result is discussed in the contest of the possible occurrence of self-compatibility of J. mimosifolia. The low level of incongruity operating between the two species also points to their recent evolutionary divergence.
... However, pollen imports perhaps had less impact on the selection of J. rugosa's staminode, once it does not ensure reproductive success since only one fruit is formed for every 18 pollinated flowers according to our estimate. This occurs because the species seems to be subject to a strong limitation of female function as observed in most Jacaranda species (Vieira et al., 1992;Guimarães et al., 2008;Maués et al., 2008;Milet-Pinheiro & Schlindwein, 2009b;Bittencourt, 2019) and other Bignoniaceae (Bittencourt & Semir, 2004;2005;Gandolphi & Bittencourt, 2010;Alves et al., 2013;Bittencourt et al., 2003Bittencourt et al., , 2011Sampaio et al., 2016). In addition, the proportion of fruits formed was lower than the proportion of stigmas with only intraspecific pollen. ...
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The floral traits in Bignoniaceae are claimed as precise determiners of specialized pollination systems. Here, we investigated how such floral traits ensure a highly specialized interaction between Jacaranda rugosa and medium-sized bees by examining visual, and olfactory signaling, as well as mechanical fit to pollinating bees. We also report the efficiency of the system by fitness measures (pollen delivery from anthers; pollen deposition on stigma; fruit and seed set). Jacaranda rugosa probably attracting bees through chromatic and achromatic contrasts of staminode with corolla and pollen mimicry, and floral volatile compounds that are common to other bee-pollinated systems. Fundamental and realized accuracy ensure tight mechanical fit to medium-sized bees. While the natural female component is strongly limited, promoting lower fruit set than pollinated flowers, the floral morphology seems to ensure high male fitness by pollen transfer. Our results demonstrate that floral traits of J. rugosa promote a specialized system for pollination by medium-sized bees, and this process is likely to happen in other species of Bignoniaceae or flowers with similar traits.
... Data on crop production, dependence on pollinators, and the main crop-pollinator species are scarce for the Amazon biome. Furthermore, our knowledge about pollination in AFSs in Brazil is limited (but see Maués and Santos, 1999;Maués et al., 2000;Maués and Couturier, 2002;Maués et al., 2008;Oliveira and Schlindwein, 2009;Dáttilo et al., 2012;Cavalcante, 2013;Bezerra et al., 2020), which demonstrates the large knowledge gap that exists in pollination and agroforestry practice. An example is cocoa, a commodity with high production value and scarce knowledge about its effective pollinators (Paz et al., 2021), especially in the Amazon (the main producer in Brazil). ...
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With the growing demand for food production worldwide, natural landscapes are increasingly being replaced by agricultural areas, which directly affects biodiversity and local ecosystem services. Agroforestry systems, which are the intentional integration of trees and shrubs into crop and animal farming systems, are a more sustainable production approach that has been increasing in several forested areas around the globe. Here, we examine the trends of agroforestry in the Brazilian Legal Amazon and estimate the associated value of ecosystem services mediated by pollinators. Using data from 2006 and 2017, we detected an increase in agroforestry activity in the Amazon, both in the number (3.27%) and in the area (23.18%) of establishments. Crop production in forested areas increased by 45.61% in the same period, and the main products cultivated in both years were native products from the Amazon, such as açaí , Brazil nut and babassu. Although the crop data are from forested areas, all the five crops with the highest production value are associated with agroforestry in the Amazon. Pollination services also increased during the same period from US$73.3 to US$156.7 million (113.76%). In 2006, the value of pollination services corresponded to 44% of the total crop production, and it jumped to 64.43% in 2017. Bees and beetles were the two main groups of pollinators quoted for the analysed crops. Our estimates show the important contribution of pollinators to crop production in the Amazon forest. However, a growing loss of Amazon forest has been observed, and this can jeopardize pollinators and have detrimental consequences on food production in the near future. Public policies are urgently needed to encourage crop production in harmony with natural areas, combining the protection of forests and pollinators with food production.
... They described operation in many plant species of self-incompatibility systems (SI) that operate in the ovary, naming this phenomenon late-acting SI systems (Seavey and Bawa, 1986). Contrary to SI mechanisms that inhibit pollen germination and pollen tube growth, late-acting SI inhibit pollen tube growth in the ovary before it reaches the ovule, or may cause the post-zygotic rejection of the developing embryo (Bittencourt and Semir, 2005;Maués et al., 2008). Late-acting SI may explain the patterns of seed production within the pod of Bauhinia ungulata (Bawa and Webb, 1984;Rocha, 2005a, 2005b;Webb and Bawa, 1985) where the rejection of seed development can be regarded as a way of controlling maternal investment through selective seed abortion. ...
Article
The Organization for Tropical Studies (OTS) has played a pivotal role in our understanding of tropical ecosystems' structure and function. For more than fifty years, OTS has contributed to the training of three generations of tropical biologists and facilitated, supported, and promoted leading-edge research in its field stations. Plant reproductive ecology and genetics have been a significant focus of OTS research since the early 1960s, and Dr. K.S. Bawa made a significant contribution to the advancement of this field. His work improved our understanding of the diversity and evolution of breeding systems in tropical forests, their phenology and pollination ecology, and their mating and genetic structure. We argue that his work inspired other tropical biologists' work and used the work of one of the authors for illustration when appropriate. We point out the need for research in critically important topics to slow down biodiversity loss, prevent the collapse of tropical systems in a changing climate, and the emergence of zoonotic disease. We suggest future research topics for the OTS field stations, including in plant reproductive biology.
... Pollination biology of Penstemon haydenii of Scrophulariaceae suggested that open pollinated flowers produced significantly fewer seeds per fruit than that of the experimental out crossing treatment and this is due to low pollinator efficiency (Tepedino et al., 2007). The floral biology, breeding system and pollinators of Jacaranda copaia of the family Bignoniaceae has been investigated (Maues et al., 2008). It has been reported that species in an obligate allogamous. ...
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Editorial 'Muses' is an anthology of nine researches of several academicians, each working in different spheres. Proceeding along different tracks, traversing flora and fauna, through 'crops' and 'venom', 'silk' and 'heavy metals', they like most researches, ultimately converge to make a full life and a complete existence. They are all attempts to discover, analyze, reflect or review our stand on myriad issues which contribute to our very being. The outcome is then this fascinating web-a miniature life-our 'Muses.' In Greek mythology, the Nine Muses are the inspirational deities of literature, sciences and the arts, urging human minds to creativity, for centuries. Legends say that all ancient writers appealed to the Muses at the initiation of their work. Homer asks the Muses both in the Iliad and Odyssey to help him narrate the tales in the most befitting manner. Till today the Muses have remained symbols of inspiration, encouragement, creation and life beyond the ordinary. The 1 st Volume of 'Muses' owes its birth to several such inspired minds without whom this journey would not even have been conceived. With deep gratitude and respect, I acknowledge them all. We look to our readers for further analyses and critiques. 'Muses' now belongs to them… Happy Reading and Much
... suggested that secretions from glandular trichomes of staminodia attract pollinators, and that the physical location of staminodia in flowers play a role in increased pollinator contact with reproductive organs (Guimarães et al., 2008). Most species in Jacarandeae seem to be pollinated by euglossine bees (Gentry, 1974;Guimarães et al., 2008;Maues et al., 2008;Milet-Pinheiro and Schlindwein, 2009). Endlicher (1839) described three sections within Jacaranda based on number of anther thecae and calyx morphology: (1) Copaia with one anther sac and tubular, truncate calyces; (2) Hemilobos with one anther sac and campanulate, five-lobed calyces; and (3) Dilobos with two anther sacs and campanulate calyces. ...
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Premise: The tribe Jacarandeae includes Jacaranda (49 species) and Digomphia (3 species), two genera of trees and woody shrubs with Neotropical distribution. Jacarandeae is sister to the rest of the Bignoniaceae, but not much is known about interspecific and intergeneric relationships within this group. Methods: We reconstructed the phylogeny of Jacarandeae using chloroplast (ndhF, rpl32-trnL, trnL-F) and nuclear (ETS, PPR62) markers. Evolutionary relationships within Jacarandeae were inferred using Bayesian, Maximum Likelihood, and species tree approaches. The resulting phylogenetic framework was used as the basis to interpret the evolution of key morphological character states (i.e., stamen and calyx traits) and revise the infra-generic classification of the group. Results: Jacaranda and Digomphia belong to a well-supported clade, with Digomphia nested within Jacaranda. We propose the necessary taxonomic changes to recognize monophyletic taxa, including a broadly circumscribed Jacaranda divided into four sections: (1) Jacaranda sect. Nematopogon, species previously included in Digomphia and united by divided staminode apices and spathaceous calyces; (2) Jacaranda sect. Copaia, species with monothecal anthers and cupular calyces; (3) Jacaranda sect. Jacaranda, species with monothecal anthers and campanulate calyces; and (4) Jacaranda sect. Dilobos, species with dithecal anthers and cupular calyces, and including more than half of the species of the genus, all restricted to Brazil. Conclusions: As circumscribed here, Jacarandeae includes only a broadly defined Jacaranda divided into four sections. Each section is defined by a unique combination of anther and calyx morphologies.
... The causes of this variation in nectar production rhythm in J. oxyphylla flowers are yet unknown. Most beepollinated Bignoniaceae species start nectar production before anthesis (Galetto, 1995;Lopes et al., 2002;Maués et al., 2008;Guimarães et al., 2016;Quinalha et al., 2017;Souza et al., 2017), so that pollinators have high probability of finding nectar in freshly opened flowers. However, in J. oxyphylla, when searching for nectar in recently opened flowers, pollinators have a 78% chance of finding empty flowers, considering that 47% of flowers are nectarless and 31% start nectar release just in the second day of anthesis ('late' flowers). ...
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The presence of nectarless flowers in nectariferous plants is a widespread phenomenon in angiosperms. However, the frequency and distribution of nectarless flowers in natural populations, and the transition from nectariferous to nectarless flowers are poorly known. Variation in nectar production may affect mutualism stability, since energetic resource availability influences pollinators’ foraging behavior. Here, we described the spatial and temporal nectar production patterns of Jacaranda oxyphylla, a bee-pollinated species that naturally presents nectarless flowers. Additionally, we compared nectariferous and nectarless floral disks in order to identify histological, subcellular and chemical changes that accompanied the loss of nectar production ability. For that we used standard methods for light and transmission electron microscopy, and gas chromatography coupled to mass spectrometry for chemical analyses. We verified that 47% of flowers did not produce nectar during the whole flower lifespan (nectarless flowers). We also observed remarkable inter-plant variation, with individuals having only nectarless flowers, others only nectariferous ones and most of them showing different proportions of both flower types, with variable nectar volumes (3–21 μl). Additionally, among nectariferous flowers, we registered two distinct rhythms of nectar production. ‘Early’ flowers produced nectar from 0 to 24 h, and ‘late’ flowers produced nectar from 24 to 48 h of anthesis. Although disks from nectariferous and nectarless flowers displayed similar histological organization, they differed strongly at subcellular level. Nectariferous (‘early’ and ‘late’) flowers exhibited a cellular apparatus typical of nectar secretion, while nectarless flowers exhibited osmophoric features. We found three aliphatic and one aromatic compound(s) that were detected in both the headspace of flowers and the disks of nectarless flowers, but not the disks of nectariferous flowers Although the remarkable variation in nectar availability may discourage pollinator visits, nectarless flowers might compensate it by producing volatile compounds that can be part of floral scent, acting as chemical attractants. Thus, nectarless flowers may be helping to maintain pollination in this scenario of trophic resource supply scarcity. We suggest that J. oxyphylla can be transitioning from a nectar-based pollination system to another resource-based or even to a deceit mechanism of pollination.
... We checked the species distribution recorded in our research with information available on the literature for Neotropical region (Dressler, 1982a, b, c;Hinojosa-Díaz and Engel, 2014;Oliveira, 2006;Ramírez et al., 2002;, Brazilian Amazon (Nemésio and Morato, 2004;2006;Nemésio, 2005;Oliveira and Campos, 1995;Oliveira and Nemésio, 2003;Santos-Júnior et al., 2014;Storck-Tonon et al., 2009;; Atlantic Forest and Cerrado (Nemésio, 2009;2010;2012b;Nemésio and Silveira, 2007;2010;Nemésio and Faria-Junior, 2004;Oliveira-Junior et al., 2015;and Silva, 2012); and current studies carried out on the states of Pará and Maranhão (Antonini et al., 2017;Brito et al., 2017; Brito and Rêgo, Maués et al., 2008;Rebêlo and Cabral, 1997;Silva and Rebêlo, 1999;Solar et al., 2016). We found one species with new record for BEC. ...
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The distribution of most species occurs in delimited regions with unique characteristics called “centers of endemism”. In Eastern Amazon is located the Belém Endemism Center (BEC), one of the most intensely deforested in Brazilian Amazon. Here, we show information about orchid bee assemblages based on historical records from entomological collections. For each species, we calculated occurrence frequency and dominance, and we classified them in 3 statuses: common, intermediate or rare species. Curves of observed and estimated richness were built, based on Jackknife estimator. We found 1,257 specimens from 56 species, constituting records from 1917 to 2009, and one species is a new record for BEC. Higher number of specimens and species was concentrated in a few locations and surveys increased from the 70’s. The results suggest a high richness of orchid bees in the BEC, although this scenario is far from what is expected for the entire area. The high occurrence of rare species may be related to their low representativeness in the collections, and the proximity between the areas had favored samplings. Even so, the species list and the conservation status presented here may be useful information in studies comparing past and current orchid bee fauna, and, allied to data on bees’ responses to land use changes occurred in BEC over the years, can fit as a basis for defining priority areas for conservation.
... Entre las especies neotropicales y de regiones templadas, la biología reproductiva exhibe una apreciable diversidad, ya sea en el tipo de sistema reproductivo como en patrones fenológicos (Gentry, 1974a,b) y tipos morfológicos florales (Gentry, 1974b). La mayoría de las especies presenta autoincompatibilidad y xenogamia obligada (Stephenson & Thomas 1977;Bertin, 1982;Weber & Vogel, 1986;Gentry, 1990;James & Knox, 1993;Gibbs & Bianchi, 1993Bittencourt Jr. et al., 2003;Bittencourt Jr. & Semir, 2004;Rodrigues Correia et al., 2005;Motta Maués et al., 2008;Gandolphi & Bittencourt Jr., 2010); aunque en menor frecuencia fue mencionada la presencia de cierto grado de autocompatibilidad (Gobatto-Rodriguez & Stort, 1992;Dutra & Machado, 2001). En numerosas especies con polinización cruzada fue comprobada la existencia de algún mecanismo de autoincompatibilidad de acción retrasada (LSI, late-acting self-incompatibility) (Bittencourt Jr. et al., 2003). ...
Article
Few studies directly address the consequences of habitat fragmentation for communities of pollinating insects, particularly for the key pollinator group, bees (Hymenoptera: Apiformes). Bees typically live in habitats where nesting substrates and bloom are patchily distributed and spatially dissociated. Bee studies have all defined habitat fragments as remnant patches of floral hosts or forests, overlooking the nesting needs of bees. Several authors conclude that habitat fragmentation is broadly deleterious, but their own data show that some native species proliferate in sampled fragments. Other studies report greater densities and comparable diversities of native bees at flowers in some fragment size classes relative to undisrupted habitats, but find dramatic shifts in species composition. Insightful studies of habitat fragmentation and bees will consider fragmentation, alteration, and loss of nesting habitats, not just patches of forage plants, as well as the permeability of the surrounding matrix to interpatch movement. Inasmuch as the floral associations and nesting habits of bees are often attributes of species or subgenera, ecological interpretations hinge on authoritative identifications. Study designs must accommodate statistical problems associated with bee community samples, especially non-normal data and frequent zero values. The spatial scale of fragmentation must be appreciated: bees of medium body size can regularly fly 1-2 km from nest site to forage patch. Overall, evidence for prolonged persistence of substantial diversity and abundances of native bee communities in habitat fragments of modest size promises practical solutions for maintaining bee populations. Provided that reserve selection, design, and management can address the foraging and nesting needs of bees, networks of even small reserves may hold hope for sustaining considerable pollinator diversity and the ecological services pollinators provide.
Article
As human influences on natural systems extend to the furthest reaches of the planet, a challenge for the twenty-first century is how to reconcile resource use with an equitable and just quality of life for current and future generations of people, while also conserving the millions of other species with which we share the planet. This is especially relevant for tropical regions known to be biodiversity rich. The question is how, exactly, this should be accomplished, and what measurements can be used to establish whether the goal has been reached. This article describes the Dendrogene Project, an initiative developed to provide tools for improving conservation values in managed forests in the Brazilian Amazon and to contribute to the sustainable development of the region's natural resources. Such a blend of conservation and management is seen by many as the lasting solution to the region's problems of poverty and inequality. The project, hosted at the Eastern Amazon research station of the Brazilian Agricultural Research Corporation (Embrapa), focuses on providing skills and tools to forest users so that knowledge-based management systems can be applied in practice. A forest simulation model is being developed to analyse alternative scenarios of forest use. The simulation modelling approach makes it possible to test criteria and indicators for the sustainability of genetic and ecological processes in managed forests.