Isabel Cristina Machado

Fruiting phenology and seed dispersal syndromes in caatinga, a tropical dry forest in the northeast of Brazil

This study describes the fruiting phenology of woody plants and their dispersal syndromes in caatinga (semi-arid region in the northeast of Brazil). The fruiting phenology of 42 species with different dispersal modes and life-forms was followed over a period of 1 y. Animal dispersal was the most commonly observed dispersal mode (36%), followed by anemochory (33%), ballistic dispersal (19%) and barochory (12%). Overall, a greater number of species fruited during the rainy season. Zoochorous species were the most representative in the rainy season, whereas anemochorous species predominated during the dry season. Five different life-forms were observed, and the occurrence of dispersal modes was discussed for each of them. In the caatinga plant community studied the patterns of life-forms, fruiting phenology and seed dispersal syndromes were similar to other tropical seasonal ecosystems. Este trabalho teve como objetivo principal descrever como se comportam as especies de caatinga (regiao semi-arida do Nordeste brasileiro) com relacao ao modo de dispersao durante as estacoes seca e chuvosa. Foram observados tambem os modos de dispersao apresentados em cada forma de vida. A fenofase de frutificacao foi acompanhada em 10 individuos de 42 especies durante um intervalo de um ano. A zoocoria representou o modo de dispersao mais observado (36%), seguido da anemocoria (33%), balistica (19%) e barocoria (12%). Um maior numero de especies frutificou durante a estacao de chuvas, sendo a zoocoria mais representativa nesta estacao, enquanto que a anemocoria foi mais representativa na epoca de estiagem. Foram observadas varias formas de vida, discutindo-se o modo de dispersao em cada uma delas. Constatou-se que as especies de caatinga estudadas encontram-se dentro dos padroes gerais de epoca de dispersao dos diasporos e representatividade das sindromes de dispersao observados em outros ecossistemas com sazonalidade.

SISTEMA DE POLINIZAÇÃO E REPRODUÇÃO DE BYRSONIMA SERICEA DC (MALPIGHIACEAE)

A polinizacao, o sistema reprodutivo e a fenologia de floracao de Byrsonima sericea, foram estudados no periodo de outubro/1997 a fevereiro/1998 na Reserva Ecologica de Dois Irmaos, Recife (PE). Byrsonima sericea possui porte arboreo (3 a 20m), com periodo de floracao de outubro a fevereiro. As flores sao hermafroditas, zigomorfas, agrupadas em inflorescencias do tipo racemo terminal. A corola e amarela e possui cinco petalas unguiculadas, sendo a superior modificada em forma de estandarte. O calice e formado por cinco sepalas com dez glândulas epiteliais produtoras de oleo, os elaioforos. Em alguns individuos essas glândulas sao ausentes. O androceu e formado por dez estames, com anteras rimosas e deiscencia ocorrendo em fase de pre-antese floral. A viabilidade dos graos de polen foi de 93,3% e 98,3%, em individuos com e sem elaioforos, respectivamente, sendo o numero de graos de polen por antera de 1.216,66 e 923,33 e a razao polen/ovulo (P/O) de 308.000 e 405.500. Como visitantes das flores, observaram-se abelhas pertencentes as familias Anthophoridae (coletoras de oleo e polen), Apidae e Halictidae (somente polen). Baseando-se nas estrategias e recompensas florais (oleo e polen), elevada razao P/O e, principalmente, na ausencia de formacao de frutos nos experimentos de autopolinizacao, conclui-se que esta especie e xenogama.

Pollination of Campanula rapunculus L. (Campanulaceae): How much pollen flows into pollination and into reproduction of oligolectic pollinators?

Abstract.We studied an isolated population of Campanula rapunculus and two oligolectic bee species of Chelostoma (Megachilidae), their main pollinators. The population of C. rapunculus consisted of 2808 plants. Measurements of pollen flow showed that 3.7% of the pollen produced by a flower contribute to pollination, 95.5% was collected by bees for their offspring and 0.8% remained on the styles. Pollen analyses of brood cells of Chelostoma rapunculi revealed that females collected on average 4.9 million Campanula pollen to rear one bee. We calculated that approximately 1588 bees of this species could have been reared at the study site during the studied season. The amount of potentially viable pollen deposited on stigmas was 3.6 to 10.7 times higher than the number of ovules. We discuss morphological features of the flowers which may lower the pollen removal rate per bee visit and consequently cause a high visitation and pollination rate.

Pollination of four sympatric species ofAngelonia (Scrophulariaceae) by oil-collecting bees in NE. Brazil

The manner whereby the oil-producing bisaccate flowers ofAngelonia (Scrophulariaceae) are pollinated by female oil-collecting bees is reported for the first time. Observations were made in the Caatinga formation of Pernambuco, NE. Brazil, on four synchronopatric species. These differ in sizes and structural details of the corolla, level of flower exposition, and habitat preferences. All legitimate visitors wereCentris spp. (Anthophoridae):Angelonia hirta was mainly pollinated byC. fuscata andA. pubescens byC. hyptidis; A. bisaccata andA. hookeriana shared an unidentified species. Several exomalopsine, tetrapediine and meliponid bees exploit the flowers less descriminately for oil or pollen, respectively, without regularly contacting anthers and stigma. The flowers are protandrous, and are self-incompatible except those of the annualA. pubescens. After alighting, theCentris bees introduce their front legs simultaneously into each of the pouches and start alternate collecting movements to gather the oil from the trichome elaiophores. While doing so, they are forced by projections of the corolla floor to press their head under the anthers and stigma, whereby pollen is transferred with their frons or clypeus. On account of their collector type and behaviour,C. fuscata andC. spec. are not specialized toAngelonia but may equally exploit other nonrelated taxa for oil, whereasC. hyptidis exhibits oligolecty onA. pubescens. It possesses relatively elongate forelegs with padlike collectors suitable for sweeping the lipids from the scattered glandular hairs inside the divergent spurs of its host. It is the only species that also collects pollen (by buzzing) from the oil host.A. hirta and relatives, provided with dense elaiophore carpets, are, for their part, adapted to “scraping”Centris species with typical oil collectors. Flower and bee phenologies, although largely dependent on the irregular rainfalls, are not always coincident.

Floral biology and reproductive ecology ofClusia nemorosa (Clusiaceae) in northeastern Brazil

Between March 1993 and May 1995 the floral biology and the phenology ofClusia nemorosaG. Mey. (Clusiaceae) were studied in two dioecious populations in Pernambuco State, and some observations were made in gynodioecious populations, that were encountered only in Bahia State. The species flowers from June to January/February. The flowers are bowl shaped, and last only one day. The floral reward is resin which is produced by staminodia in all types of flowers. The sex ratio was 1:1 for the studied populations. The pollen viability was approximately 98%. Apomixis was not observed. The rate of fruit set, in hermaphrodite individuals, under natural conditions and the sex ratio of the gynodioecious populations studied suggest that the hermaphrodite individuals may behave as males.Clusia nemorosa is melittophilous and was visited by 16 species of bees. The main pollinators wereEuplusia mussitans, E. iopyhrra, Eulaema cingulata, E. nigrita, Euglossa cordata andEuglossa sp.

Bat pollination of the terrestrial herbIrlbachia alata (Gentianaceae) in northeastern Brazil

The pollination of the terrestrial herbIrlbachia alata by the batGlossophaga soricina was recorded in northeastern Brazil. This herb colonizes disturbed swampy sites in clearings and forest edges, blooming year-round. Its greenish white flowers open at dusk and attract phyllostomid bats and hawkmoths. The long-tongued batGlossophaga soricina is the major pollinator ofI. alata at the study site, with its trapline visits promoting cross-pollination of this herb. The small flowers and the delicate stem ofI. alata match the small size and the manoeuverable flight of glossophagine bats.

Biologia da polinização e sistema reprodutivo de Psychotria barbiflora DC. (Rubiaceae)

The reproductive biology of Psychotria barbiflora was investigated from April/1999 to September/2000, in the Dois Irmaos State Park, Recife, Pernambuco State, Brazil, an Atlantic Forest remnant. Psychotria barbiflora is a understory species (0.5-2.0m tall), which flowered between April and July and fruiting from June to September. The species presented heterostyly (distyly), and the flowers are arranged in terminal, pendant inflorescences, wrapped in bracts, which are greenish during the flowering period and become purple during the fruiting phase. Anthesis began at about 4:30 a.m. and the flowers last until 1:00 p.m. Recorded nectar volume were c. 0.80 and 0.60µl and sugar concentration was approximately 22 and 24%, respectively, in long and short-styled flowers. The floral morphs were similar in corola size but short-styled flowers had larger, less numerous pollen grains when compared to long-styled ones. Psychotria barbiflora is a mellitophylous species, pollinated by three bee species which were observed collecting nectar and pollen, and also by a wasp species, which collected only nectar, in both floral morphs. Based on the results of hand-pollination tests and observations of pollen-tube growth, it can be concluded that this species has sporophytic self-incompatibility.

Biologia reprodutiva de Canistrum aurantiacum E. Morren (Bromeliaceae) em remanescente da Floresta Atlântica, Nordeste do Brasil

Canistrum aurantiacum, a shade-tolerant species, is either an epiphyte or a terrestrial plant, endemic of the coastal Atlantic forest understory from Pernambuco and Alagoas. The species forms dense terrestrial populations, flowering from November to mid-February with the peak of flowering in the last half of January, when 12 flowers per plant may open during one day. The flowers are tubular and vary from 4-5 cm in length within the same inflorescence. The flowers begin to open from the centre of the inflorescence and progress towards the periphery. C. aurantiacum is an ornithophilous species, whose syndrome is characterised by odourless flowers, vivid-red involucral and scape bracts, and golden-yellow corolla. Nectar volume varies from 22,6 to 40,5 ml, with concentration of 26-33 %. Anthesis begins at dawn, around 5:20 a.m. and the flowers close around 4:00 p.m. Pollen and stigma are functional during the whole anthesis. Hummingbirds Chlorostilbon aureoventris and Thalurania watertonii (Trochilinae), Glaucis hirsuta, Phaethornis pretrei and P. ruber (Phaethornitinae) visited the flowers. The last one could be considered as the main pollinator, and was seen at regular intervals of 10 to 30 minutes, typical of the trap-lining visiting pattern. C. aurantiacum is a self-compatible species, nevertheless it produces low number of seeds per fruit in self-pollination treatments compared to the natural pollinations promoted by hummingbirds. Pipra rubrocapilla (Pipridae) and Tangara faustuosa (Thraupinae) were observed dispersing the fruits of C. aurantiacum. Ornithophily predominates in the Bromeliaceae, and has been characterised as a parallel evolution mechanism between bromeliads and hummingbirds. Canistrum aurantiacum is a typical example of this close relationship.

Pollination and seed dispersal of Melocactus ernestii Vaupel subsp. ernestii (Cactaceae) by lizards: an example of double mutualism

Recent studies show that the mutualistic role of lizards as pollinators and seed dispersers has been underestimated, with several ecological factors promoting such plant-animal interactions, especially on oceanic islands. Our aim is to provide a quantitative assessment of pollination and seed dispersal mutualisms with lizards in continental xeric habitats. We carried out focal observations of natural populations of Melocactus ernestii (Cactaceae) in the Caatinga, a Brazilian semiarid ecosystem, in order to record the frequency of visits, kind of resource searched and behaviour of visiting animals towards flowers and/or fruits. We made a new record of the lizard Tropidurus semitaeniatus foraging on flowers and fruits of M. ernestii. During the search for nectar, T. semitaeniatus contacted the reproductive structures of the flowers and transported pollen attached to its snout. Nectar production started at 14:00 h, with an average volume of 24.4 μl and an average concentration of solutes of 33%. Approximately 80% of the seeds of M. ernestii found in the faeces of T. semitaeniatus germinated under natural conditions. The roles of T. semitaeniatus as pollinator and seed disperser for M. ernestii show a clear relationship of double mutualism between two endemic species, which may result from the environmental conditions to which both species are subject. Seasonality, low water availability and arthropod supply in the environment, high local lizard densities, continuous nectar production by the flower and fruits with juicy pulp may be influencing the visits and, consequently, pollination and seed dispersal by lizards in this cactus.

Fenologia reprodutiva e sistema de polinização de Ziziphus joazeiro Mart. (Rhamnaceae): atuação de Apis mellifera e de visitantes florais autóctones como polinizadores

(Reproductive phenology and pollination system of Ziziphus joazeiro Mart. (Rhamnaceae): the role of Apis mellifera and autochthonous floral visitors as pollinators). Ziziphus joazeiro is an endemic species of the Caatinga with great economic importance, whose reproductive biology is poorly understood. This paper analyses the reproductive phenology, floral biology and pollination system of Ziziphus joazeiro at Cariri Paraibano, northeastern Brazil. Flowering and fruiting periods occurred at the end of the dry season and beginning of the rainy season, with peaks in December (flowering) and February (fruiting). The green, dish-shaped flowers last about 12 hours and have a large yellow nectary surrounding the gynoecium. Protandry occurs associated with heterodichogamy, another type of dichogamy. Ziziphus joazeiro produces little nectar (1 µl) but with a high sugar concentration (75%). Floral visitors were wasps, bees and flies. Apis mellifera had the highest frequency of visits (77.5%), followed by wasps (20.4%), both acting as effective pollinators. Flies and other bee species had a lower percentage of visits (2.1%) and acted as nectar robbers. The high rate of initial fruit development per inflorescence suggests high pollinator efficiency, since the dichogamic mechanism prevents the occurrence of spontaneous self-pollination and geitonogamy.