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Tropical Biology |
2Institute of Systematic Botany, The New York Botanical Garden, Bronx, New York 10458-5126 USA; 3Jardin Botanique, Place Bardineau, F-33000 Bordeaux, France; 4Laboratoire d'Ecologie Générale, UMR 8571 CNRS-MNHN, 4 Avenue du Petit Château, 91800 Brunoy, France
Received for publication June 25, 2002. Accepted for publication October 24, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: bat dispersal • Cecropia • French Guiana • fruit anatomy • fruit morphology • mucilage • Neotropical bats • soil seed bank
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), plays several important ecological roles in tropical forest ecosystems. One of the best studied is the mutualistic interaction among species of Cecropia and ants of the genus Azteca (Davidson, in press). Nearly 80% of the species of Cecropia are myrmecophytes with most of the non-myrmecophytes found at higher elevations and on islands where the ants are absent (Wheeler, 1942
; Janzen, 1973
; Rickson, 1977
). Myrmecophytic species of Cecropia possess hollow stems, in which ants nest, and provide an energy source for the ants in the form of glycogen-rich Müllerian bodies found at the base of the petiole on a specialized structure called a trichilium. In return, the ants protect the plant against phytophagous insects and from competition by other plants (Davidson, in press).
Another important ecological role played by species of Cecropia is as pioneer plants in disturbed areas. An individual Cecropia can yield fruits for 4–5 mo, and some species of the genus produce seeds capable of germinating after 4 or 5 yr of dormancy (Holthuijzen and Boerboom, 1982
; Charles-Dominique, 1986
; Lescure et al., 1989
). An example of the prolific seed-producing capacity is Cecropia obtusifolia, an abundant pioneer species found in Mexico, which reliably fruits each year. This species produces a mean of 80.6 ± 22.8 infructescences per tree per fruiting episode with each infructescence consisting of four rachises and an estimated 2792 seeds per rachis (Estrada et al., 1984a
). Estrada et al. (1984a)
calculated that a total of 900 141 seeds were produced by each female tree at each fruiting. As a result of this productivity, seeds of Cecropia are often the most common in soil seed banks in both primary and secondary forests (Whitmore, 1983
). For example, along the Piste de St. Elie in French Guiana, seeds of C. obtusa and C. sciadophylla may account for 50% of the soil seed bank in primary forest (Prévost, 1982
). Because of the abundance of seeds in the soil, as well as the rapid dispersal of them into newly disturbed areas, regeneration of forests in gaps is facilitated by species of Cecropia throughout most of the Neotropics.
Trees of Cecropia often produce the first shade and litter, which enables later successional species to germinate and establish seedlings in disturbed areas (Maury-Lechon, 1991
). Although Cecropia species have little economic value (Berg and Franco-Roselli, in press
), they appear to play an essential role in initial stages of plant succession after disturbance. At least in French Guiana, Cecropia often provide the microhabitat needed for the growth of economically important timber trees such as Goupia glabra and Laetia procera (Maury-Lechon, 1991
).
In all species of Cecropia, the fruits are surrounded by a perianth that becomes fleshy and serves as a reward to animal dispersal agents. The infructescences of species of Cecropia are exploited by many different species of vertebrates: various birds, bats, monkeys, fish, and others (Holthuijzen, 1979
; Goulding, 1980
; Charles-Dominique et al., 1981
; van Roosmalen, 1985
). Hence, the infructescences of species of Cecropia are an important source of nutrition for many Neotropical animals.
In spite of the numerous studies about the dispersal biology of Cecropia, there is still confusion in the literature about what is dispersed (i.e., the definition of the diaspore) and what part of the infructescence is consumed by animals. In addition, the morphology and anatomy of the fruits and seeds of Cecropia have not yet been adequately described. Therefore, we undertook this study to (1) examine the role that bats play in the dispersal of Cecropia, (2) establish what is the dispersal unit (diaspore) of Cecropia, (3) determine what part of the infructescence is consumed by animals, (4) provide the first botanical descriptions of the fruit and seed morphology and anatomy of bat-dispersed Cecropia species native to French Guiana, (5) ascertain if there are differences in the diaspores of bat-dispersed Cecropia species that can be used to identify species from material collected from bat feces, (6) investigate what structural changes occur in the diaspores of Cecropia after passing through the digestive tract of bats and after burial in the soil seed bank, and (7) determine the role that fruit structure of Cecropia plays in seed longevity in the soil seed bank. Seven species of Cecropia are found in French Guiana (C. distachya Huber, C. granvilleana C. C. Berg, C. latiloba Miq., C. obtusa Trécul., C. palmata Willd., C. sciadophylla Mart., and possibly C. silvae C. C. Berg) (Berg and Franco-Roselli, in press
). It is the bat-dispersed species of Cecropia that are the focus of our research.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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).
Fruits and seeds were collected from bat feces on six expeditions to French Guiana (July–August, 1999; August–September, 2000; October–December, 2000; February–May, 2001; April–May, 2001; and July–December, 2001). Bats were captured in primary and secondary forest in ground level mist nets and placed in clean cloth bags until they had defecated. The fruits and seeds from the feces were then air dried in glassine envelopes. A total of 936 fecal samples with fruits/seeds was gathered. The bats carrying the seeds were identified using Neotropical Rainforest Mammals (Emmons, 1990
) and then released unharmed.
Fruits from herbarium specimens of species of Cecropia were compared with fruits from feces of bats. Herbarium vouchers are deposited in the herbaria of The New York Botanical Garden (NY) and the Institut de Recherche pour le Développement (CAY). Fruit/seed collections from bat feces are archived at The New York Botanical Garden and CNRS (Muséum National d'Histoire Naturelle, France).
Fruit morphology and anatomy of the following species were studied (vouchers of herbarium or bat feces collections in parentheses): Cecropia obtusa (Smith and Mori 20, herbarium specimen; Peckham 191/1999, Charles-Dominique 662, Charles-Dominique 752, from bat feces); C. palmata (Berg 784, herbarium specimen; Charles-Dominique s. n., from bat feces); C. sciadophylla (Mori 18749, herbarium specimen; Peckham 209/2000, Peckham 211/2000, from bat feces).
Several fruits of C. obtusa collected from bat feces (Charles-Dominique 662, Charles-Dominique 752) were deposited in the seed soil bank at Les Nouragues Research Station in French Guiana. Fruits in nylon mesh bags were buried 3 cm deep at one site with clay soil and at another site with sandy soil. After 1 yr in the soil, the morphology and anatomy of these fruits were compared with fruits that had passed through the digestive tracts of bats.
For morphological studies, dry fruits and seeds, and longitudinal and transverse sections of fruits sputter-coated with gold-palladium were examined with a JEOL 5410LV scanning electron microscope (SEM; Jeol USA, Peabody, Massachusetts, USA). For anatomical studies, dry fruits were softened for 7 d in a solution of equal parts distilled water, 96% ethanol, and glycerol. Transverse sections (12 µm thick) were cut in the middle of the fruits using a freezing microtome. Histochemical reactions were made with Sudan IV, phloroglucinol + HCl, and IKI to determine the presence of lipids, lignin, and starch, respectively (Jensen, 1962
). A polarizing filter was used to detect crystals and starch grains. Fruits were placed in tap water and observed for mucilage after 24 h.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and for bats (Nowak, 1994
), our review of the literature revealed reports of 15 species of Cecropia consumed by 32 species of bats (Table 1). In French Guiana, only C. obtusa (Foresta et al., 1984
; Cooper and Charles-Dominique, 1985
; Charles-Dominique, 1986
, 1993
; Charles-Dominique and Cooper, 1986
; Cockle, 1997
), C. palmata (Charles-Dominique, 1986
), and C. sciadophylla (Cockle, 1997
) have been reported to be bat-dispersed (Table 1). Among the 936 fecal samples we collected with fruits/seeds, 162 contained the fruits of Cecropia (Table 2).
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Fruits of C. obtusa were found in 135 samples of feces gathered from bats captured both in primary and secondary vegetation (Table 2). The infructescences are consumed by Artibeus obscurus (fruits found in 41 samples), A. jamaicensis (40), A. lituratus (20), Sturnira tildae (16), Carollia perspicillata (4), Platyrrhinus helleri (4), Artibeus concolor (3), Sturnira lilium (2), Artibeus gnomus (1), A. cinereus (1), Carollia brevicauda (1), Chiroderma villosum (1), and Platyrrhinus brachycephalus (1).
We have observed three intensities of pericarp abrasion in the fruits of C. obtusa after passage through the digestive tract of bats (Figs. 2, 4). Most of the fruits lose the mucilaginous cells of the exocarp, some lose only part of the mucilaginous cells with those left maintaining the ability to produce mucilage when placed in water, and others lose the entire exocarp as well as part of the outer mesocarp.
Fruits of C. obtusa collected from bat feces and experimentally placed in the soil seed bank had not undergone significant additional structural changes after 1 yr (Figs. 10, 11). The exocarp of all fruits was completely missing as the result of passage through the digestive tract of bats. Fruits buried in clay soil are reddish brown because of the adhesion of clay particles to their surface, while those buried in sandy soil are whitish brown as a result of the loss of tannins from the cells of the outer mesocarp (Fig. 11). The latter color change is probably caused by the higher acidity of sandy soils in comparison to clay soils. Tannins are not dissolved in water, but are removed by acidic solutions (Johansen, 1940
; Schmid, 1977
).
Description of fruits and seeds: Cecropia palmata
Fruits obovoid to oblong, ca. 2 x 1.3 x 0.7 mm, whitish-yellow, glossy, the basal end roundish, the apical end more or less flat, obtuse; transverse section triangular-rounded, or elliptic; surface tuberculate (Figs. 16–18, 21), the tubercles small; mucilage layer ca. 0.06 mm thick exudes after placement of fruits in water. Pedicel scar conspicuous, basal-lateral, elliptic; vascular bundle single, in one lateral side. Pericarp (Figs. 20, 21) ca. 150 µm thick, thicker in lateral sides, thinner in middle of dorsal and ventral sides, with 6–14 layers, differentiated into exocarp, mesocarp, and endocarp (Fig. 22). Exocarp single-layered, with two cell types (Fig. 14): first large mucilaginous, with thin anticlinal walls and thickened outer periclinal walls, considerably elongated without destruction of cell boundaries when wet, the second cell type non-mucilaginous, much smaller, with thicker walls, filled with light brown pigment; non-mucilaginous cells rare and situated on top of tubercles. Mesocarp 4–12 layers, differentiated into three zones (Figs. 14, 22): outer zone of single layer of small cells with thickened non-lignified walls; intermediate zone of 2–10 (more in lateral sides) layers of longitudinally elongated macrosclereids with lamellar thickened walls; inner zone a single layer of cells, each with a prismatic crystal 6.5–9 µm in diameter. Endocarp occupying one-half to two-thirds of pericarp, a single layer of radially elongated macrosclereids, longer in tubercles, the macrosclereids similar to those of pericarp of C. obtusa (Figs. 14, 22).
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After passing through the digestive tract of a bat, the fruits of C. palmata lose some of the mucilaginous cells of the exocarp (Figs. 17, 19). The remaining cells retained their ability to produce mucilage when placed in water.
Description of fruits and seeds: Cecropia sciadophylla
Fruits ellipsoid, ca. 2.9 x 1.2 x 0.9 mm, dark brown, glossy, the end(s) acute; transverse section triangular-rounded or elliptic; surface tuberculate, the tubercles smaller or absent on ends (Figs. 26–28, 31); mucilage layer ca. 0.1 mm thick exudes after placement of fruits in water. Pedicel scar conspicuous, basal, circular; vascular bundle single, in one lateral side. Pericarp (Figs. 30, 31) ca. 160–200 µm thick, thicker in lateral sides, thinner in middle of dorsal and ventral sides, with 5–8 layers, differentiated into exocarp, mesocarp, and endocarp (Fig. 32). Exocarp single-layered, with two cell types (Figs. 15, 32): first large mucilaginous, with thin anticlinal walls and thickened outer periclinal walls, considerably elongated without destruction of cell boundaries when wet, the second cell type non-mucilaginous, much smaller, with thicker walls, filled with brown pigment; non-mucilaginous cells situated on tubercles, the mucilaginous cells between them. Mesocarp 3–6 layers, differentiated into two zones (Figs. 15, 32): outer zone 2–5 (more in tubercles) layers of longitudinally elongated tanniniferous cells, the walls slightly thickened, the outer periclinal walls of first layer thicker; inner zone a single layer of cells, each with a prismatic crystal 6.5–13 µm in diameter. Endocarp occupying one-half to two-thirds of pericarp, a single layer of radially elongated macrosclereids, longer in tubercles, the macrosclereids similar to those of pericarp of C. obtusa (Figs. 15, 32).
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After passing through the digestive tract of a bat, the fruits of C. sciadophylla lose all or part of their exocarp (Figs. 27, 29). The remaining mucilaginous cells retained their ability to produce mucilage when placed in water.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Artibeus lituratus, the largest South American frugivorous bat, has been calculated to eat 144 g, nearly double its body mass (Charles-Dominque et al., 2001
), of C. obtusa per night. Because A. lituratus does not eat large quantities of insects, most of its nutrients come from fruits. The dry mature infructescences of C. obtusa in French Guiana contain approximately 50% fruits, 25% non-hydrosoluble fibers, and a 25% hydrosoluble fraction consisting mostly of C6 and C12 sugars and 0.4–0.6% nitrogen, represented by 21 free amino acids (Charles-Dominique, 1986
). The infructescences of C. obtusa contains 2.2 mg/g dry pulp (derived from the perianth) of free amino acids (0.22%) and 45.5 mg/g dry pulp of soluble sugars (4.55%). The infructescences of C. sciadophylla have a similar composition of amino acids and sugars. The relatively low nutrient content is compensated for by the fact that bats eat a lot of infructescences (Charles-Dominique, 1986
).
In search of fruit, Artibeus lituratus makes approximately 40 feeding flights per night; and, as in many species of frugivorous bats, fruit passage through the gut is as short as 5 min when the bat is actively foraging (Charles-Dominique and Cooper, 1986
). Examination of 212 fecal samples from Artibeus lituratus, Sturnira lilium, and Carollia perspicillata by Charles-Dominique and Cooper (1986)
revealed the presence of fruits of C. obtusa in 10 of 19 samples, 1 of 41 samples, and 0 of 152 samples from each species of bat, respectively. Artibeus lituratus, therefore, preferentially feeds on C. obtusa, but documentation of this is difficult to obtain because this bat flies relatively high in the canopy, i.e., above the level that most nets are set (Charles-Dominique, 1986
).
Bats play an important role in moving the diaspores of secondary forest species into primary forest (Table 2) and in transporting the larger seeds of primary forest into secondary forest. Artibeus lituratus, for example, consumes the seeds of the secondary forest species Cecropia obtusa (Tables 1, 2), as well as the fruits of the primary forest species Symphonia globulifera, Licania spp., Parinari spp., Caryocar glabrum, Dipteryx odorata, Bocoa prouacensis, and Swartzia panacoco (Foresta et al., 1984
; Charles-Dominique and Cooper, 1986
). The seeds of these species are relatively large, but this bat is capable of transporting fruits and seeds almost as large as itself (Foresta et al., 1984
).
Radio tracking of Artibeus lituratus in French Guiana (Foresta et al., 1984
) has demonstrated that this species feeds in fruiting trees within a radius of 200–400 m and that it changes feeding patches 2–3 times a night. The patches may be 1–2 km apart from one another. Moreover, this bat can have its day roosts in primary forest as well as in or close to secondary forest. Consequently, Artibeus lituratus plays a role in the movement of at least one secondary forest species, Cecropia obtusa, into primary forest and can potentially transport the seeds of a number of primary forest species into secondary forest. In a study of bat dispersal of C. obtusa, Charles-Dominique (1986)
found that bats visiting this species sometimes arrived with the fruits of primary forest species such as Licania sp. and Symphonia globulifera. In Mexico, Vásquez-Yanes et al. (1975)
found that Artibeus jamaicensis also transported seeds between primary and secondary vegetation. Measurement of the seed rain in primary forest in French Guiana using eight 1-m2 plots yielded a total of 2864 fruits and seeds during the course of a year. Among the propagules were 1111 fruits of C. obtusa (139 fruits · m–2 · <011>yr–1) and 25 fruits of C. sciadophylla (3.1 fruits · m–2 · <011>yr–1) (P. Charles-Dominique, unpublished data).
Although bats commonly consume the infructescences of species of Cecropia, many other animals exploit this abundant resource. The murine mouse opossum, Marmosa murina, has been photographed eating a fragment of an infructescence of Cecropia sp. and fruits of C. palmata have been found in its digestive tract (Charles-Dominique et al., 1981
). The primate Alouatta palliata consumes the fruits of C. obtusifolia in the area of Los Tuxtlas, Mexico (Estrada et al., 1984b
) and the fruits of C. peltata in Costa Rica (Fleming and Williams, 1990
). But this howler monkey feeds on unripe infructescences and therefore should be considered a seed predator as well as potential seed disperser (Fleming and Williams, 1990
). Estrada et al., (1984a)
observed 48 different species of animals consuming the infructescences of C. obtusifolia. Kinkajous and marsupials seek the infructescences of C. obtusa in French Guiana (Charles-Dominique, 1986
; Julien-Laferrière, 2001
). Charles-Dominique (1986)
observed that the tiny arboreal rodent Oecomys bicolor consumes the unripe fruits of C. obtusa and C. sciadophylla, and, hence, it is a seed predator rather than a seed disperser. Additionally, at least 76 species of birds in 19 families are known to feed on Cecropia (Holthuijzen, 1979
). Fleming and Williams (1990)
documented that in a Costa Rican tropical dry forest diurnal and nocturnal animals consume similar amounts of C. peltata fruits and suggested that the digestive systems of birds and bats treat Cecropia fruits more gently than do monkeys.
Earlier work on C. obtusa and C. sciadophylla has suggested that some species of Cecropia are adapted for dispersal primarily by birds and others primarily by bats (Charles-Dominique, 1986
; Charles-Dominique and Cooper, 1986
). Although fruit of C. obtusa is mostly dispersed by bats, birds (e.g., Thraupis spp., Ramphoceles carbo, and Pteroglossus spp.) remove 17% of the fruits during the day (Charles-Dominique, 1986
). In contrast, the fruits of C. sciadophylla are usually dispersed by birds (Charles-Dominique et al., 1981
; Foresta et al., 1984
; Charles-Dominique, 1986
, 1993
; Charles-Dominique and Cooper, 1986
). Nevertheless, Cloutier and Thomas (1992)
, Gorchov et al. (1995)
, and Cockle (1997)
have identified fruits of C. sciadophylla in the feces of species of Artibeus, Carollia, Phyllostomus, and Rhinophylla (Table 1).
In our study, fruits of C. sciadophylla were obtained only from Rhinophylla pumilio on three occasions (Table 2), supporting Cockle's (1997)
findings that R. pumilio at least occasionally consumes the infructescences of C. sciadophylla in French Guiana. Our collections are the first documentation of the consumption of the infructescences of C. obtusa by Artibeus obscurus, A. gnomus, A. cinereus, Carollia perspicillata, C. brevicauda, Chiroderma villosum, Platyrhinnus helleri, P. brachycephalus, Sturnira tildae and the infructescences of C. palmata by A. obscurus and P. helleri.
Diaspores of Cecropia
In all species of Cecropia, the fruits are achenes surrounded by enlarged perianths aggregated into digitate infructescences (Berg and Franco-Roselli, in press
). We do not consider the fruit to be a sorosus (compound fruit) in the sense of Spjut (1994)
because the fruit is not fleshy; moreover, there are no fusions among adjacent perianths or between the perianth and the fruit. Fruits of C. obtusa, C. palmata, and C. sciadophylla are easily removed from the perianth when fresh or dry. During germination, the pericarp splits along the lateral sides into two equal parts to expose the seed (T. Lobova, unpublished data). Because the fruits are small, indehiscent, and one-seeded, they are referred to as seeds in most of the bat/plant literature. However, the diaspores of species of Cecropia are technically fruits, so bats (as well as other animals) disperse fruits and the soil seed bank contains fruits. Bats consume the ripe parts of an infructescence, digest the pulp derived from the enlarged, fleshy perianth and defecate the fruits.
We assume, therefore, that the "fruit nutritional content" of Cecropia reported in the literature refers to the nutritional content of the persistent perianth. Because dispersal agents digest no part of the fruit, fruits should be removed from the perianth, and only the nutritional composition of the perianth should be assayed in future studies.
Comparison of fruit structure
The fruits of C. obtusa, C. palmata, and C. sciadophylla all produce mucilage when placed in water and are morphologically and anatomically similar. In these three species, the pericarp is thick, the exocarp contains both mucilaginous and non-mucilaginous cells, the mesocarp has a crystal-bearing inner layer, and the endocarp consists of large macrosclerids (Figs. 13–15). The same general pericarp structure was described by Kravtsova (1995)
for C. distachya Huber, C. membranacea Trécul., C. obtusifolia Bertoloni, C. pachystachya Trécul., C. peltata L., and C. schreberiana Miq. Species-specific pericarp characters for C. obtusa are the rugose surface and presence of an intermediate stone cells zone in the mesocarp, for C. palmata the small tubercles, the presence of an outer cell layer with non-lignified walls and macrosclereids in the mesocarp, and the lack of tannins in the pericarp, and for C. sciadophylla the large tubercles and absence of sclereids in the mesocarp. Size, color, shape, and surface provide other characters that can be used to identify these species based on material collected from bat feces (Table 3). We conclude that the fruits of these and some other species (Kravtsova, 1995
) of Cecropia possess the interspecific variation needed for identifying fruits in plant/animal studies. Moreover, we suggest that morphological and anatomical characters of fruit may be useful in the species taxonomy of Cecropia.
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; Hutchinson, 1967
).
Significance of external mucilage production
The ecological functions of the external production of mucilage in fruits and seeds has been hypothesized to (1) aid in water retention during germination; (2) fix the diaspore to the soil or other substrates; (3) lubricate the radicle as it penetrates the soil; (4) increase diffusion of water from the substrate into the seed; (5) facilitate hydrochory; (6) enhance epizoochory by increasing the ability of diaspores to adhere to animals; (7) build an additional protective barrier by promoting adhesion of soil particles to the diaspore; and (8) prevent the germination of seeds under water-logged conditions by hindering oxygen uptake (Haberlandt, 1914
; Murbeck, 1919
; Gill, 1935
; Harper and Benton, 1966
; Gutterman et al., 1967
, 1973
; Kuijt, 1969
; Witztum et al., 1969
; Fahn and Werker, 1972
; Grubert, 1974
; Werker, 1997
). The significance of mucilage to endozoochorously dispersed diaspores has not been broadly discussed in the literature.
The fruits of C. obtusa, C. palmata, and C. sciadophylla partly or entirely lose the mucilaginous part of the exocarp while passing through the digestive tracts of bats (Figs. 4, 19, 29). We consider this to be the result of moisture absorption by the fruits combined with mechanical and/or chemical abrasion during passage. Fruits that have been placed in water followed by air drying display almost the same fruit surface pattern as those that have passed through the digestive tracts of bats. Species-specific differences in the original size and extent of mucilaginous cells play a role in the degree of change the fruit surface displays. Thus, C. obtusa and C. sciadophylla, which produce a mucilage layer 0.1 mm thick, undergo considerably more exocarp destruction (Figs. 4, 29) than C. palmata, with a mucilage layer only 0.06 mm thick (Fig. 19). However, because infructescences are consumed in pieces, the fruits are differentially protected depending on their position in relation to the remaining parts of the infructescence as they pass through the digestive tracts of bats. These differences may account for the variable amount of change seen in pericarp of fruits from feces within each species.
Kravtsova (1995)
noted the presence of a mucilaginous exocarp in the fruits of Cecropia distachya, C. membranacea, C. obtusifolia, C. pachystachya, C. peltata, and C. schreberiana. All these species are also reported to be dispersed by bats (Table 1).
It seems unlikely that mucilage is nutritionally important to bats because the fruits of Cecropia produce an insignificant amount of it. Moreover, the mucilaginous cells are often intact after passing through the bat's intestines, whereas the perianth surrounding the fruit is completely digested. Nevertheless, the nutritional content of the mucilage of Cecropia has not been determined. We suggest that mucilage covering the fruit of Cecropia provides lubrication and thereby promotes fruit passage through the digestive tracts of animals.
Influence of bats on dispersal and seed germination
Diaspores pass through the digestive tracts of bats within 5–20 min (Fleming and Heithaus, 1981
; Charles-Dominique, 1986
). This short passage time lessens the amount of mechanically and chemically induced changes suffered by the diaspores. The passage removes the perianth and all or part of the mucilaginous layer surrounding the fruit of Cecropia, thereby reducing the adhesion of fruits with one another. Because bats defecate in flight, the fruits from a single defecation are spread over a surface of about 2–3 m long and 0.5–1 m wide (P. Charles-Dominique, unpublished data). Therefore, bat dispersal of Cecropia provides efficient dissemination into large gaps and primary forest.
Endozoochorous dispersal may increase the germination of many seeds owing to the removal of an impermeable layer of the seed coat and/or a soluble germination inhibitor (van der Pijl, 1972
; Traveset and Verdú, 2002
). Estrada with coauthors (Estrada et al., 1984a
; Estrada and Coates-Estrada, 1986
) observed that fruits of Cecropia obtusifolia after passage through the digestive tracts of animals have greater germination than fruits not consumed by animals. Fleming (1988)
found similar results for C. peltata. In contrast, Vázquez-Yanes and Orozco-Segovia (1986)
, in their study of C. obtusifolia, concluded that passage through the digestive tracts of bats did not influence seed germination.
In our germination experiments with C. obtusa (T. Lobova, unpublished data), we obtained 100% seed germination after 10–15 d from fruits taken from 2-yr-old herbarium specimens and 100% germination after 30–35 d from fruits taken from a 2-yr-old bat fecal sample (fruits kept in tap water at room temperature under ambient office light). These observations support the findings (Vázquez-Yanes and Orozco-Segovia, 1986
) that passage of the fruits of Cecropia through the digestive tracts of bats is not necessary for seed germination. In addition, these findings suggest that external mucilage production does not play a significant role in the germination of Cecropia seeds as they germinate with or without mucilage in nature or in the laboratory.
We consider, however, that removal of tissue surrounding the diaspore, whether it is the result of passing through the digestive tract of a bat or because of a controlled experiment, is probably essential for optimum seed germination. Estrada et al., (1984a)
reported that whole infructescences of C. obtusifolia fallen on to the forest floor were rapidly attacked by fungi, and the seeds did not germinate. Under these circumstances, the intact perianth may have prevented the penetration of the light needed for germination. Also, under excessively moist conditions, the fleshy perianth and the mucilaginous layers of the diaspores can serve as a substrate for bacterial growth, which results in seed rot (Gutterman et al., 1973
). We conclude that fruit passage through a bat's digestive tract increases seed survival and enhances germination by removing the perianth and some of the mucilaginous tissue from the fruits.
Role of fruit structure in seed longevity
As mentioned previously, the fruits of C. obtusa and C. sciadophylla are among the most common in the soil seed bank (Prévost, 1982
). At two sites in French Guiana, one in primary forest and another in primary forest close to secondary forest, fruits of C. obtusa were found at densities of 50 fruits/m2 and 70 fruits/m2 and fruits of C. sciadophylla at densities of 28 fruits/m2 and 32 fruits/m2 to a depth of 3 cm, respectively (P. Charles-Dominique, unpublished data). Seeds of Cecropia can germinate after 4, 5 (Holthuijzen and Boerboom, 1982
; Charles-Dominique, 1986
; Lescure et al., 1989
) or even up to 9 yr after dispersal (P. Charles-Dominique, unpublished data).
Ecological longevity of seeds in tropical rain forest is among the shortest of any plant community because seeds tend to germinate soon after dispersal (Foster, 1986
; Garwood, 1989
; Vazquez-Yanes and Orozco-Segovia, 1993
). Delayed germination, a feature of species found in soil seed banks, exposes diaspores to the diverse population of year-round predators and parasites common to environments with high soil moisture and temperature (Foster, 1986
; Vazquez-Yanes and Orozco-Segovia, 1993
). Factors that independently, or in combination, may extend the longevity of seeds in forest soil are (1) the presence of a dormancy mechanism that prevents rapid germination; (2) the presence of a hard and/or impermeable coat that prevents rehydration and diminishes predation; and (3) the presence of strong chemical defenses against parasitism and predation (Janzen et al., 1982
; Hopkins and Graham, 1987
; Alvarez-Buylla and Martinez-Ramos, 1990
; Vazquez-Yanes and Orozco-Segovia, 1993
; Baskin and Baskin, 1998
). The diaspores of Cecropia meet these requirements. First, they possess an efficient dormancy mechanism, requiring light for germination (Holthuijzen and Boerboom, 1982
; Vazquez-Yanes and Orozco-Segovia, 1986
; Souza and Válio, 2001
). In addition, our study of the fruit anatomy of C. obtusa, C. palmata, and C. sciadophylla reveals a number of features that may enhance seed longevity in the soil seed bank. These species have a hard and somewhat impermeable pericarp consisting of a very thick inner sclerefied layer, support from a crystal-bearing layer, and additional sclereids in the mesocarp of C. obtusa and C. palmata. Furthermore, the pericarps of C. obtusa and C. sciadophylla have a layer of tanniniferous cells. Tannins protect seeds from attack by herbivores, fungi, bacteria, and viruses (Roth, 1987
) and may also make the cell layers containing them harder and impermeable to water (Rangaswamy and Nandakumar, 1985
). Nevertheless, the fruits of Cecropia are not completely impermeable because the vascular bundle penetrates the pericarp at the pedicel scar. Evidence of the efficacy of these structures is that fruits of C. obtusa that have been in the soil seed bank for a year have not changed from those collected from the feces of bats. An exception, however, is the disappearance of tannins from the pericarps of fruits that are taken from the seed banks of sandy, presumably more acidic, soils.
We conclude that the fruits of Cecropia have evolved features that allow them to remain dormant in the soil seed bank until conditions become favorable for seed germination. These features make it possible for species of Cecropia to play an essential role in forest regeneration after disturbance. The occurrence of stands of Cecropia in many large and small gaps throughout the Neotropics reflects the fruit adaptations of this ecologically successful pioneer species.
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FOOTNOTES |
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), which has been made possible through financial support of the Beneficia Foundation and Bat Conservation International. 
5 Author for reprint requests (phone: 718 817-8833; FAX: 718 817-8648; tlobova{at}nybg.org
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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