Ecological Distribution of Chlorophyllous Developing Embryos among Perennial Plants in a Tropical Deciduous Forest
1982; Wiley; Volume: 14; Issue: 3 Linguagem: Inglês
10.2307/2388030
ISSN1744-7429
Autores Tópico(s)Agronomic Practices and Intercropping Systems
ResumoA dry-season survey of the developing seeds of 74 species of Costa Rican deciduous forest perennial plants found that the developing embryos of 55 percent of the species were highly chlorophyllous; these species had flat, strap-like or cylindrical fruits with seeds less than 1 g mature weight, or had fully insolated spheroidal fruits with four or less smallto mediumsized seeds. The achlorophyllous seeds were in fruits with large seeds, fruits with many seeds packed in layers, or in fruits borne in locally shady habitats. The presence of a chlorophyllous developing embryo would seem to add significant complexity to the already-complex parasite-host relationship of the embryos that are developing in the fruit, in that fruit and seed-coat traits are evolutionarily affected by transmission of light to the embryo and a phytosynthetic embryo may be able to develop more independently of the parent than can an achlorophyllous embryo. THE DEVELOPING EMBRYOS of many species of plants are deep green due to the presence of chlorophyll and chloroplasts similar to those of leaves (Dah1gren 1980, Yakovlev and Zhukova 1980). In plants with dormant seeds, the chlorophyllous embryos become achlorophyllous upon maturing and remain that way during seed dormancy, suggesting that the chlorophyllous state is of value to the developing embryo, rather than simply being an early stage of seedling development. If this is so, there should be ecological correlates with chlorophyllous seeds. I surveyed the developing seeds and associated fruit traits in 74 species of native perennial shrubs, trees, and lianas in the middle of the dry season in a Costa Rican lowland deciduous forest (Santa Rosa National Park, northwestern Guanacaste Province) and found three such correlates. The species were chosen by virtue of being all those that I could find bearing green fruits during a three-day period (8-10 March 1980). The embryos (cotyledons plus radicle, hypocotyl, etc.) of 55 percent of the species were intense leafgreen during a long portion of their development. Chlorophyllous embryos were found in all species that bore fully insolated fruits that were flat, straplike or cylindrical with smallto medium-sized seeds of less than 1 g mature weight, and in almost all highly insolated spheroidal fruits with four or less smallto medium-sized seeds (fig. la-e; table 1). An instructive exception was Lantana camara, which had fruits that were small, green, single-seeded spheres (2-4 mm diameter) that matured in full sunlight, yet the developing embryos were never green. However, the fruits were arranged in a tight cluster, and therefore the entire infrutescence was similar to a single large fruit with many small seeds scattered through it. The embryos of 45 percent of the species were never chlofrophyllous (table 1). These species had very large seeds (e.g., Dioclea megacarpa (fig. lg), Andira inermis, Saprarnthus palanga, Acrocomia vinifera), had many seeds packed in several layers in spheroidal or thick cylindrical fruits (e.g., Apeiba tibourbou (fig lf), Carica papaya, Sapranthus palanga, Crescentia alata, Tabebuja rosea, Brassavola nodosa), or grew in locally shaded habitats (e.g., Ardisia revoluta, Aphelandra deppeana (fig. lh), Hirtella racemosa). Additionally, the achlorophyllous embryos of two sapindaceous species had deep-green seed coats and therefore could be said to live in a heavily shaded microhabitat. In all other species surveyed (72), the developing seed coats were translucent white and the developing fruits were leaf-green. The mature and dormant seeds of all 74 of the surveyed species are achlorophyllous. It is clear that chlorophyllous-developing embryos are found in strongly insolated developing fruits, fruits with all the seeds about equally close to the surface, and fruits and seeds thin or small enough that light penetrates to the embryo. This conclusion constitutes an alternative hypothesis to the view (Dahlgren 1980, Yakovlev and Zhukova 1980) that the presence of chlorophyllous embryos is a family-level trait dependent on taxonomic rather than ecological circumstances. Studies of pho,tosynthate production and allocation by fruits of trees (Bazzaz et al. 1979) and crop herbs (Andrews and Svec 1975, Atkins and Flinn 1978, Atkins et al. 1977, Biscoe et al. 1975, Crookston et al. 1974, Elmore 1973, Enyi 1962, Flinn and Pate 1970, Flinn et al. 1977, Harvey et al. 1976, Hedley et al. 1975, Johnson et al 1975, Kriedemann 1966, Lovell and Lovell 1970, Quebedeaux and Chollet 1975, Sambo 1977, Thorne 1965, Wilmer and Johnston 1976) show clearly that a fruit may contribute 232 BIOTROPICA 14(3): 232-236 1982 This content downloaded from 157.55.39.120 on Mon, 05 Sep 2016 05:51:12 UTC All use subject to http://about.jstor.org/terms ~ ~ ~ ~~~~~~~ ~~~ ~~~~~~~~~~~~~~~~~~~~~~~ -1111 :0: 11_ l FIGURE 1 A. Full-sized green fruit of Enterolobium cyclocarpum with partial section to expose nearly full-sized green embryos B close-up of section in (A) showing dark-green embryo (cotyledon) sectioned longitudinally within white, translucent seed coat within white mesophyll next to green pericarp (bottom). C. Intact bright-green, immature, full-sized fruit of Caesalpinia exostemma (top), fruit split open to show intact seeds with translucent seed coat (middle), and longitudinally sectioned fruit to show dark-green embryos (cotyledons) in full-sized, immature seeds. D. Partly mature fruit of Caesalpinia coriaria longitudinally sectioned to show nearly mature seeds with whitening embryos (cotyledons) (upper two seeds) and less-mature seeds with green embryos (two seeds on lower right), and clear endosperm (between elongate thin embryos and seed coats). E. Nearly mature fruit of Rourea glabra (upper) and section through less-mature fruit showing green cotyledons and white fruit pulp (aril). F. Nearly mature, bright-green fruit of Apeiba tibourbou (left) and section through fruit (right) showing white, mature seeds imbedded in a brownish-yellow matrix. G. Maturing fruit of Dioclea megacarpa split open with one seed split (left) to show white insides. H. Sections through fruits of Aphelandra deppeana to show white, young seeds (left) and white, nearly mature seeds (right). All fruits from the lowland, deciduous forests of Santa Rosa National Park, northwestern Costa Rica, March 1980 (all scales in millimeters). a non-trivial fraction of the material used to develop and fill a seed. However, they do not show what fraction of this photosynthetic activity is performed by chlorophyllous embryos and what fraction by maternral fruit tissue. This distinction is important because a fruit is parasite(s) and host combined in one complex structure. The offspring live in such a resource-limited environment that even very small amounts of resources from their own photosynthesis are likely to be of proportionately large value. When the developing embryo is chlorophyllous, several variables are added to the already-complex interaction between the fruit and seeds. Fruit and seed shape are under selection to increase exposure of cotyledonary tissues; as fruit walls thicken or seeds become thicker in response to other selective pressures, a cost is incurred through deprivation of a chlorophyllous embryo of sunlight. The seeds packed into a spheroidal or thickly cylindrical fruit deprive each other of light. Fruit-developmental timing should also be influenced by chlorophyllous embryos; even rainyseason, cloudy daylight is adequate for photosynthesis Ecological Distribution of Chlorophyllous Embryos 233 This content downloaded from 157.55.39.120 on Mon, 05 Sep 2016 05:51:12 UTC All use subject to http://about.jstor.org/terms TABLE 1. Traits of 74 species of developing wild perennial plant fruits recorded on 8-10 March 1980 (mid dry season) in the lowland deciduous forests of Santa Rosa National Park, northwestern Guanacaste Province, Costa Rica. Approximate Seed weight number of +=>1 g Fruit shape seeds -=<1 g CHLOROPHYLLOUS EMBRYOS Anacardiaceae Astronium graveolens Cylinder 1 Burseraceae Bursera simaruba Angular sphere 1 Combretaceae Combretum farinosum. 4-bladed flat disk 1 Terminalia chiriquensis Flat disk 1 Connaraceae Rourea glabra Ovoid sphere 1 Convolvulaceae Ipomoea carnea Angular sphere 4 Merremia umbellata Sphere 4 Merremia cissoides Angular sphere 4 Hippocrateaceae Hemiangum excelsum Broad-blade propeller 2-4 Leguminosea: Acacia collinsii Flattened cylinder 8-15 Acacia farnesiana Cylinder 10-15 Ateleia herbert-smithii Flat disk 1 Bauhinia ungulata Flat strap 5-10 Caesalpinia exostemma Flat strap 3-5 Caesalpinia coriaria S-loop flat strap 2-5 Cassia biflora Flat strap 5-15 Cassia emarginata Flat strap 20-40 Cassia hayesiana Cylinder 20-30 Centrosema plumieri Flat strap 6-10 Centrosema pubescens Flat strap 6-15 Crotalaria maypurensis Cylinder 10-15 Desmanthus virgatus Flat strap 10-15 Enterolobium cyclocarpum Flat disk 5-20 + Gliriczdia sepium Flat strap 3-10 Haematoxylon brasiletto Flat strap 1-4 Piscidium carthagenensis 4-bladed flat strap 1-4 Pithecellobium saman Flat strap 5-20 Phaseolus lunatus Flat strap 2-5 Prosopis juliflora Undulating flat strap 10-15 Pterocarpus rohrii Flat disc 1 Malpighiaceae Banisteriopsis cornifolia Samara 1 Malvaceae Malvaviscus arboreus Sphere 3-6 Ochnaceae Ouratea lucens Ovoid sphere 1 Polygonaceae Coccoloba venosa Sphere 1 Triplaris melaenodendron Shuttlecock 1 Rosaceae Licania arborea Ovoid 1 -+ Rubiaceae Calycophyllum candidissimum Cylinder 1 Sapindaceae Serjania schiedeana Samara 1 Thouinidium decandrum Samara 1 Simaroubaceae Picramnia quaternaria Ovoid sphere 1 Simarouba glauca Flattened sphere 1 +
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