| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Tropical Biology |
Smithsonian Tropical Research Institute, Apartado 2072, Ancón, Balboa, Republic of Panama
Received for publication November 10, 2000. Accepted for publication February 15, 2001.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: androdioecy • inflorescence structure • Moraceae • Panama • pollination • thrips
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
; Rohwer, 1993
). The most important trend of evolution of inflorescences may be progressive condensation by fusion and reduction of floral parts (Rohwer, 1993
), which can be associated with reduction of flowers and change from bisexual to unisexual condition (Berg, 1989
). This tendency appears to be most tightly linked with protection of flowers from destructive organisms that consume or cause infection of floral tissues. The interactions that minimize loss to such floral parasites may in some cases lead to mutualism (Berg, 1989
). In the case of Ficus, seed predators have evolved into pollinators of the plant (Bronstein and McKey, 1989
; Herre et al., 1996
; Anstett, Hossaert-McKey, and Kjellberg, 1997
). In Artocarpus integer, male inflorescences infected by fungi provide mycelia as a reward for gall-midge pollinators (Sakai, Kato, and Nagamasu, 2000)
. It is remarkable, however, that little is known about pollination systems in the Moraceae other than Ficus and some apparently wind-pollinated species (Berg, 1989
; Endress, 1994
; Rohwer, 1993
). Several available studies suggested that various pollination systems are involved (Bawa et al., 1985
; Momose et al., 1998
; Sakai, Kato, and Nagamasu, 2000
) and that wind-pollination might have evolved more than once (Zapata and Arroyo, 1978
; Bawa and Crisp, 1980
; Williams and Adam, 1993
; Bullock, 1994
).
Here, I report on the pollination system of Castilla elastica Sessé (Moraceae). Although the species was formally important for rubber production and was cultivated in the late 1800s and early 1900s (Pittier, 1910
; Hammel, 1986
), its reproductive biology is poorly studied. Three forms of inflorescences, the most peculiar characteristic of the species, were described by Cook (1903a, b)
for the first time. Cook (1903a, b)
and Pittier (1910)
examined living and preserved materials as well as dry specimens and mentioned that the species was "partly dioecious" with two types of trees within a population. There were trees that bore only male inflorescences, while others produced pistillate inflorescences flanked by a few staminate inflorescences, which were smaller than primary ones. The stamens on both types of trees were fertile (Pittier, 1910
). In other words, the species was androdioecious.
As theoretical studies have predicted (Charlesworth and Charlesworth, 1978
) androdioecy (cosexes and males in a single population) is an extremely rare sexual system in plants (Charlesworth, 1984
). In most androdioecious species reported so far, a cosexual individual produces hermaphrodite flowers (Datisca spp. [Datiscaceae] [Liston, Rieseberg, and Elias, 1989
; Swensen, Luthi, and Rieseberg, 1998
], Fraxinus spp. and Phillyrea angustifolia [Oleaceae] [Lepart and Dommée, 1992
; Yamazaki, 1993
; Hiura and Ishida, 1994
; Ishida and Hiura, 1998
; Dommée et al., 1999
], Neobuxbaumia mezcalaensis [Cactaceae] [Valiente-Banuet et al., 1997
], Oxalis suksdorfi [Oxalidaceae] [Ornduff, 1964, 1972
], Saxifraga cernua [Saxifragaceae] [Molau and Prentice, 1992
], and Schizopepon bryoniaefolius [Cucurbitaceae] [Akimoto, Fukuhara, and Kikuzawa, 1999
]). A few plant species show "monoecious" cosexes with pistillate and staminate flowers on the same inflorescences (Ricinocarpos pinifolius and Mercurialis annua [Euphorbiaceae] [Thomson et al., 1989
; Pannell, 1997
], and Sagittaria lancifolia [Alismataceae] [Muenchow, 1998
]).
Androdioecy of C. elastica is unique in that staminate and pistillate flowers occur on different inflorescences of a cosexual plant. In addition, staminate inflorescences on male and cosexual plants and pistillate inflorescences are strikingly different from one another in structure. Pistillate inflorescences are discoidal with a shallow central depression, in which pistils are aggregated (Fig. 3). Staminate inflorescences on cosexes are urceolate, "fig-like" (Cook, 1903b
) with an apical hole covered by imbricate bracts (Fig. 4), while staminate inflorescences on males are bivalvate (Fig. 2). Because of this variation and the peculiarity of inflorescence structure and the sexual system, the pollination system of Castilla was considered of particular interest.
|
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
, Pittier (1910)
, and Berg (1972)
.
Study site and plant
The study was conducted in a seasonally dry forest in the Parque Natural Metropolitano near Panama City, Panama. Annual rainfall at the site is 1740 mm on average, most of which occurs during the rainy season from May through December. The forest is 
80-yr-old second growth of 40 m in height. I used a 42 m tall tower crane with a 51-m jib at a permanent installation in the park (Parker, Smith, and Hogan, 1992
) to reach tree canopies.
Castilla elastica Sessé (Moraceae) is an abundant tree species in secondary forests and open areas such as clearings and forest edges of the region (Pittier, 1910
; Berg, 1972
). This deciduous tree can be 30 m in height. The natural distribution of the species ranges from Mexico through Panama and the coastal region of western Colombia and western Ecuador, although the species was widely spread through the tropics as a result of introduction and cultivation for its latex during the late 1800s and early 1900s (Pittier, 1910
; Berg, 1972
; Hammel, 1986
). Among the three subspecies recognized by Berg (1972)
, only C. elastica subsp. costaricana (Liebmann) C. C. Berg is known from Panama. I observed 13 reproductively mature trees within reach of the tower crane (1 ha) in April–July 2000 (Table 1).
|
Sticky traps
I used sticky traps (TAT Fly Paper; Walco-Linck, Valley Cottage, New York, USA) to compare population densities and activities of thrips among different sites. The traps catch insects on the sticky surfaces of a yellowish-brown paper (70 cm x 4.7 cm). The trap has no odor and does not contain insecticide. To compare thrips density among sites, I placed traps for 24 h in tree canopies at the height of 10–25 m and in the understory 1.5 m above the ground. The canopy traps included two traps on each of four Castilla trees (two cosexual trees, C1 and C6, and two male trees, C4 and C5) and four traps at least 10 m away from any plants flowering intensively as a control. Understory traps were placed just below each of the canopy traps. Therefore, one trapping procedure involved 24 sticky traps, and trapping was conducted twice on 27 and 28 April.
Pollination experiment
I conducted two pollination experiments on cosexual trees. In Experiment 1, I compared fruit set of inflorescences enclosed in a bag of 0.2-mm mesh, which allowed the entry and exit of tiny insects such as thrips, with that of open-pollinated control on C3. Flowers on the inflorescences were receptive around 22 April.
Experiment 2 conducted on C1 involved four treatments: (1) bagged with fine cloth; (2) hand-pollinated; (3) thrips-introduced; and (4) open-pollinated control. In the former three treatments, inflorescences were bagged with cloth fine enough to exclude thrips before the inflorescences became receptive. In addition, inflorescences were hand-pollinated with pollen of male tree C5 using a Chinese writing brush in treatment 2, and thrips collected from C5 were introduced into two bags enclosing five inflorescences each in treatment 3. Thrips for the treatment were collected from five staminate inflorescences, then released in a bag enclosing pistillate inflorescences under the treatment. This procedure was estimated to introduce 247 ± 82 thrips (98.9% of all arthropods introduced) and 2.8 ± 2.2 other arthropods (1.1%) (N = 10). Hand-pollination and thrips introduction were conducted twice on the same inflorescences on 9 and 11 May.
Fruit set was examined on 10 June by dissecting infructescences to count finished flowers and developing seeds in both experiments. At that time, infructescences (fruiting head) were still green but of almost mature size (4.3 ± 0.4 cm in diameter, N = 15). Differences in numbers of retained infructescences and in fruit set of the inflorescences between different treatments were statistically examined using Fisher's exact test and a t test, respectively, using SAS (SAS, 1988
).
Pollen staining
To examine existence of cytoplasm in pollen grains, pollen grains from frozen flower samples were dyed with methylene blue/phloxine-B solution. Phloxine-B stains cytoplasm of pollen red, and methylene blue stains the exine blue (A. Dafni, University of Haifa, Israel, personal communication).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
2.3 cm wide and 1.3 cm thick with a 0.5-cm peduncle (Fig. 2). A primary staminate inflorescence is fully packed with 400 flowers, each bearing a single stamen, on the internal surface. Anthers are 1.2 mm in length and smaller than those in complemental inflorescences (1.6 mm in length). On a branch of a cosexual tree, one or rarely two pistillate inflorescences are borne on each node. The inflorescences are almost sessile, shallow cup-shaped or discoidal with a shallow central depression, 1.0 cm thick and 1.5 cm in diameter (Fig. 3). Approximately 16 pistillate flowers on an inflorescence are fused with each other and with the receptacle at the base. At the center of the inflorescence, styles of the flowers are aggregated. The ovary is 1-locular with a single ovule. Pistillate inflorescences are usually accompanied by two or more complemental staminate inflorescences. Complemental staminate inflorescences are urceolate with a small apical opening, 1.2 cm long, and 1.0 cm in diameter with a peduncle of 1.3 cm (Fig. 4). The opening is usually blocked by imbricate bracts, but sometimes bracts are loosened during flowering, and a small hole becomes visible. A staminate inflorescence encloses 50 staminate flowers, each with a single stamen. Pollen grains are 13 µm in a diameter with three or rarely four pores. Pollen grains of male and cosexual trees each stained red by methylene blue/phloxine-B solution, indicating existence of cytoplasm in both, and there was no difference between them under a compound microscope. I could not find other rewards for pollinators besides pollen on staminate inflorescences.
The 13 C. elastica trees under observation flowered continuously or intermittently from April to May 2000. Most of their leaves had been shed before the flowering period (Fig. 1), which was followed by an explosive leaf flush. Primary inflorescences turned from green to yellow when they opened and anther dehiscence began. Within 2 d all the anthers on an inflorescence dehisced, and inflorescences then abscised. In cosexes, pistillate and staminate inflorescences were in flower simultaneously, and temporal segregation was not observed. Pistillate inflorescences changed color from green to creamy yellow as their stigma extended and probably became receptive (Fig. 3). Stigmas sometimes remained wet and fresh for >10 d. The receptive period of an inflorescence may depend on fertilization, since all the stigmas withered and turned brown <2 d after hand-pollination. Most pistillate inflorescences developed into infructescences, which reached maturity and turned salmon pink in July. The flowering period of complemental staminate inflorescences seemed to be several days, while it was difficult to examine since anther dehiscence could not be observed without damaging the inflorescence. The inflorescences had usually abscised 1 d after their color changed from green to yellow.
Flower visitors
The most abundant flower visitors were two species of thrips, Frankliniella diversa and F. insularis, both on staminate and on pistillate inflorescences (Table 2). They were observed actively feeding on pollen grains on staminate inflorescences. Many thrips emerged from primary staminate inflorescences when the branch was shaken by a breeze (Fig. 2). On pistillate inflorescences, thrips just stayed, sometimes moving around (Fig. 3). Thrips accounted for 99.0% of flower visitors (N = 1320) collected on male trees and for 99.8% (N = 450) and 96.9% (N = 32) on staminate and pistillate inflorescence of cosexes, respectively. Their sex ratio was biased in favor of female (80%, N = 1079 in F. diversa; 91%, N = 35 in F. insularis), some of which had a well-developed ovary. All thrips collected on male trees (N = 55) were observed to carry pollen grains. Seventy-one percent (N = 51) and 66% (N = 44) of thrips collected on staminate and pistillate inflorescences of cosexual trees, respectively, had pollen loads. The numbers of pollen grains on thrips collected from primary staminate inflorescences were much higher (25.8 ± 46.2 grains, N = 25) than on those from complemental inflorescences (7.6 ± 13.7, N = 51). Thrips densities on pistillate inflorescences, complemental, and primary staminate inflorescences were estimated to be 0.9 ± 1.3 (N = 59), 6 ± 4.5 (N = 7), and 202.8 ± 16.0 (N = 6), respectively.
|
), and ants (Formicidae) were observed to visit both pistillate and staminate inflorescences, but only infrequently. Ants remained on the outside of primary staminate inflorescences and on the pistillate inflorescences, catching the thrips as they entered or left the inflorescence. Beetles (Curculionidae and Staphylinidae, Coleoptera) and bees (Apidae and Halictidae, Hymenoptera) were occasionally observed visiting flowers for pollen, only on primary staminate inflorescences. High thrips activities around C. elastica were confirmed by sticky traps (Fig. 5). In the canopy traps, the numbers of thrips trapped in male trees were 33 times as high as the control. Thrips trapped in cosexual-tree canopies were also more abundant than the control, while much less than those in male trees (Fig. 5). Thrips on understory traps did not show much difference among sites. The numbers of arthropods other than thrips were almost constant at all sites both in the forest canopy and in the understory.
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Beetles and bees visited staminate inflorescences on male trees for pollen, but they were not observed on pistillate or complemental staminate inflorescences. Pistillate inflorescences or complemental staminate inflorescences closed by imbricate bracts may not be attractive for them due to absence or inaccessibility of pollen. In addition to thrips, ants and parasitoids of thrips visited both pistillate and staminate inflorescences. Although these insects might pollinate C. elastica accidentally in rare cases, they are unlikely to visit C. elastica flowers that lack their prey, thrips, and they could not be the principal pollinators, considering their low visit frequencies.
I conclude that Castilla elastica is pollinated by thrips for the following reasons. First, thrips were observed and collected on all the three types of inflorescences, primary and complemental staminate inflorescences and pistillate inflorescences, and accounted for 96.9–99.8% of the flower visitors. Presence of thrips both in staminate and in pistillate inflorescences was also observed by Pittier (1910)
. Second, a high proportion of the thrips carried pollen on the body. All the thrips collected on male trees, and two-thirds of thrips on pistillate inflorescences had pollen loads. Third, the results of the pollination experiment 1 suggest that pollen vectors included very small insects, because some flowers bagged with mesh developed into fruits. Finally, in experiment 2, thrips-introduced inflorescences enclosed in a bag of fine cloth showed fruit set as high as hand-pollinated ones and the open-pollinated control. High fruit set (80.2%) cannot be explained if thrips did not pollinate, although small numbers (1.1%) of insects other than thrips were accidentally introduced together.
Apparently, thrips visited staminate flowers for pollen. They were observed actively feeding on pollen. They probably copulated and reproduced on staminate inflorescences, because many thrips larvae as well as male and female adults were found on staminate inflorescences, and some females had developed ovaries. On the other hand, it is unclear why thrips visited pistillate flowers, which had no substantial reward. Pistillate inflorescences did not have soft tissue other than pistils, and there was no clear evidence that thrips fed upon and damaged any part of the inflorescences. Thrips might be attracted by odor and color of the pistillate inflorescences that mimic those of staminate ones. Scent is thought to be a primary attractant for thrips (Kirk, 1985
). Although I could not detect odor of pistillate flowers, volatile released by flowering inflorescences remains to be examined. Color may also be an important cue for the pollinators in C. elastica, because pistillate inflorescences changed color into yellow while flowering, although it was green before and after flowering.
Thrips, agricultural and horticultural pests causing damage by feeding on plant tissues, are often found in flowers of many wild plants (Kevan and Baker, 1983
; Kirk, 1984
). In a tropical forest of Panama, 85% of 285 species were inhabited by floral thrips (F. Gattesco, the University of Milan, Italy and D. W. Roubik, Smithsonian Institution, personal communication). Thrips feed on floral tissue, nectar and exposed liquids, and pollen grains in flowers (Kirk, 1984
). Although they are thought to rarely contribute to pollination, recent studies have reported thrips as primary pollinators in many plant species of several families including Annonaceae (Webber and Gottsberger, 1995
; Momose, Nagamitsu, and Inoue, 1998
), Araceae (Rust, 1980
), Lauraceae (Norton, 1984
), Winteraceae (Thien, 1980
; Pellmyr et al., 1990
), and Zamiaceae (Mound and Terry, 2001)
. Pollen grain size in plants pollinated by thrips is <34 µm, which corresponds well to grain size of C. elastica (F. Gattesco and D. W. Roubik, personal communication).
Host specificity of thrips varies greatly among species, and true host relationships of thrips species have rarely been established (Mound and Marullo, 1996
). Frankliniella is a large thrips genus of 180 species, 90% of which occur in the Neotropics. Its species diversity is especially high in Central America. For most species, the number of individuals collected so far is quite small. For example, among 44 species of Frankliniella recorded from Costa Rica, 18 are known only from a single sample or individual, and only ten are known from six or more samples (Mound and Marullo, 1996
). Frankliniella diversa, the most abundant thrips on C. elastica, was described based on a single female specimen from Panama; a second female was collected in Costa Rica. These two females are the only known specimens of this species prior to the present study, despite extensive collections in Central America (Mound and Palmer, 1992
; F. Gattesco and D. W. Roubik, unpublished data). The rarity might reflect host specificity of the species. A large population of F. diversa was also found on inflorescences of Poulsenia (Moraceae) (S. Sakai, unpublished data), thus they might be Moraceae specialists. On the other hand, F. insularis has been frequently collected in Panama and Costa Rica, especially from flowers of Bignoniaceae. A few individuals of this species were also collected from flowers of Bignoniaceae and Apocynaceae at the study site, when Castilla was flowering (S. Sakai, unpublished data).
Extremely high fruit set in open-pollinated flowers (Table 3), which is no lower than hand-pollinated ones, suggests the focal population of C. elastica with rather high density of flowering trees (13 trees in 1 ha) received enough pollination service. However, it is unknown how tree density affects pollination success and fruit set. Distance of thrips movement in forests has not been estimated yet. Momose, Nagamitsu, and Inoue (1998)
reported thrips pollination of an understory tree, Popowia pisocarpa (Annonaceae), and suggested that limited movement of thrips caused lower fruit set of isolated trees. On the other hand, Appanah and Chan (1981)
argued that thrips visiting flowers of emergent trees moved for long distances between trees, carried by a wind, and effectively pollinated six species of emergent trees (Shorea, Dipterocarpaceae). Observations in isolated islands and on a boat far from the land suggest that some thrips could travel >30 km (Lewis, 1973
). In C. elastica, low thrips densities on the forest floor underneath the tree canopies suggested that thrips rarely dropped with abscised staminate inflorescences. They might be dispersed by wind from canopy branches.
Sexual system
Castilla elastica is androdioecious with cosexes and male plants within a population. Pollen grains were not different between male and cosexual plants, and existence of cytoplasm was confirmed in pollen grains from both primary and complemental staminate inflorescences. However, constancy of gender expression over more than one flowering season is still unclear. Pittier (1910)
suggested that younger trees blooming for the first time might bear invariably male inflorescences, but simple size-dependent gender switching does not seem to occur, considering that no clear size difference between male and cosexual trees was found.
Theoretical studies predict that for males to invade a cosexual population, pollen success of males must be at least twice as high as cosexes; furthermore, high outcrossing rates and strong inbreeding depression are needed (Lloyd, 1975
; Charlesworth and Charlesworth, 1978
). High outcrossing rates, inbreeding depression, and pollen production by male plants observed in another androdioecious species, Datisca glomerata (Fritsch and Rieseberg, 1992
; Rieseberg et al., 1993
; Philbrick and Rieseberg, 1994
) agree with the prediction. In addition, Akimoto, Fukuhara, and Kikuzawa (1999)
showed dominance of selfing in hermaphrodite populations and significant correlation between frequency of males and inbreeding coefficients in androdioecious populations of Schizopepon bryoniaefolius. In C. elastica, male trees may have higher pollen success than cosexes, as indicated by higher thrips density on primary inflorescences than complemental ones and much higher thrips activities in male canopies than those of cosexes, as shown by data from sticky traps. Quantifying outcrossing ratio and inbreeding depression, together with sex ratio and sexual allocation, of C. elastica would be interesting problems for further studies.
A distinctive characteristic of androdioecy in C. elastica is that male and female flowers are produced on different inflorescences. Thus male and female functions do not share any structure. Additionally, the shape of staminate inflorescences on male and cosexual plants is quite different. Androdioecy in C. elastica might have evolved from dioecy. Among three Castilla species, closely related C. elastica and C. ulei are androdioecious, but C. tunu is strictly dioecious without complemental inflorescences (Berg, 1972
).
What is the advantage for cosexual plants of having staminate inflorescences? Although functionally pistillate flowers of some species are known to produce inviable pollen to attract pollinators (reviewed by Mayer and Charlesworth, 1991
), pollen concealed in urceolate complemental staminate inflorescences of C. elastica is unlikely to serve as an attractant. In C. elastica, production of staminate inflorescences causes disadvantages for cosexes in three different ways. In the first place, they should reduce production of pistillate flowers and fruits as some resources are allocated to staminate inflorescences. Second, there is the possibility that outcross pollen on pollinator bodies is lost in a complemental staminate inflorescence if thrips from other trees enter a staminate inflorescence before a pistillate one. Furthermore, complemental staminate inflorescences may increase inbreeding.
I suggest that the most likely explanation for retention of male function in cosexual C. elastica is reproductive continuity in colonists. Pollen of complemental staminate inflorescences must rarely contribute to outcrossing, because thrips in complemental staminate inflorescences were present in much lower numbers than in primary inflorescences. Pollen grains were also less abundant on thrips from complemental inflorescences, probably due to imbricate bracts blocking the entrance of the inflorescences. Outstanding colonizing ability of C. elastica is evidenced by trees growing in the wild out of its original distribution dispersed by cultivated mother trees (Berg, 1972
). Producing seeds through self-pollination must be essential when they invade a new habitat without conspecific trees. In addition, for C. elastica it may be important to assure a high level of pollination, because selective abscission of unfertilized ovaries (i.e., sterile fruits) is impossible due to fusion of all pistillate flowers on a discoid inflorescence. All flowers on a developing infructescence were observed to grow into fruits, some of which were without a seed. It may be advantageous to maintain high fruit set through self-pollination rather than to produce many seedless fruits as a part of an infructescence.
Inflorescence structure
Urceolate inflorescences occur in at least three genera of three different tribes of the Moraceae: Castilla in Castilleae, Sparattosyce in Artocarpeae, and Ficus in Ficeae. They are considered to have evolved independently for protection of reproductive organs from insects destroying reproductive organs (Corner, 1962
; Berg, 1989
). Although inflorescences, or syconia, of Ficus are clearly different from those of Castilla in that monoecious Ficus have both staminate and pistillate flowers on a single inflorescence, the pollination system of C. elastica shares some common characters with Ficus. Firstly, they are pollinated by small insects, which enter urceolate inflorescences through small holes. Host specificity of the pollinators may also be high. Next, the pollinators breed in the inflorescences. Finally, both pollination systems are possibly derived from herbivory at the inflorescence level.
Interestingly, only complemental inflorescences, rather than pistillate ones, have urceolate structure and, hence, the most closed structure in C. elastica. In contrast, the primary staminate inflorescences are opened by slits. This difference may be due to different requirements for pollinator activities. For male trees, it is essential to attract and release as many thrips as possible, while smaller complemental staminate inflorescences may function primarily to ensure self-pollination if outcross pollen is unavailable. The closed structure of a complemental inflorescence may protect pollinators as well as pollen. When there is no male tree nearby, density of pollintor thrips may be low. Therefore, a cosexual tree should increase and maintain a thrips population on its own staminate inflorescences throughout the flowering period to successfully produce seeds through self-pollination mediated by thrips. Predators of thrips such as ants and spiders were frequently observed outside of staminate inflorescences, although parasitoids were also found inside. In addition, the closed structure of staminate inflorescences promotes thrips visits to pistillate inflorescences prior to staminate ones. On the other hand, discoid pistillate inflorescences are protected by the thick receptacle, rather than closed structure. This open structure may facilitate thrips visits.
It is clear that both pollination and herbivory play important roles in the evolution of inflorescence structure of the Moraceae, although systematic relationships within the family and their pollination systems are poorly understood (Berg, 1989
; Humphries and Blackmore, 1989
). In the course of evolution, shifts from simple "floral predators" to pollinators might occur several times. These pollinators are represented by thrips in this study, the fig-wasps, that are both pollinators and seed predators of Ficus (Janzen, 1979
; Wiebes, 1979
), and gall midges pollinating Artocarpus integer, in which pollinator larvae feed on fungi infecting a staminate inflorescence (Sakai, Kato, and Nagamasu, 2000)
. Some studies on different plant groups suggest that preadaptations played essential roles in drastic changes of pollination systems, and the original function of these traits were often related to protection from destructive flower visitors (Pellmyr and Thompson, 1992
; Pellmyr et al., 1996
; Armbruster, 1997
). The Moraceae may provide interesting and unique opportunities to study the roles of nonpollinators in shaping the evolution of pollination systems.
|
FOOTNOTES |
|---|
2 Current address: Graduate School of Human and Environmental Studies, Kyoto University, Sakyo, Kyoto, Japan 606–8501 (sakai{at}bio.h.kyoto-u.ac.jp
).
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Anstett M. C. M. Hossaert-McKey F. Kjellberg 1997 Figs and fig pollinators: evolutionary conflicts in a coevolved mutualism. Trends in Ecology and Evolution 12: 94-99[CrossRef]
Appanah S. H. T. Chan 1981 Thrips: the pollinators of some dipterocarps. Malaysian Forester 44: 234-252
Armbruster W. S. 1997 Exaptations link evolution of plant–herbivore and plant–pollinator interactions: a phylogenetic inquiry. Ecology 78: 1661-1672[CrossRef][ISI]
Bawa K. S. S. H. Bullock D. R. Perry R. E. Coville M. H. Grayum 1985 Reproductive biology of a rain forest in Costa Rica. American Journal of Botany 72: 346-356[CrossRef][ISI]
Bawa K. S. J. E. Crisp 1980 Wind-pollination in the understory of a rainforest in Costa Rica. Journal of Ecology 68: 871-876[CrossRef]
Berg C. C. 1972 Olmedieae, Brosimeae (Moraceae). Flora Neotropica 7: 1-228
Berg C. C. 1989 Systematics and phylogeny of the Urticales. In P. R. Crane and S. Blackmore [eds.], Evolution, systematics, and fossil history of the Hammamelidae, vol. 2, 193–220. Clarendon Press, Oxford, UK
Bronstein J. L. D. McKey 1989 The fig–pollinator mutualism: a model system for comparative biology. Experientia 45: 601-604[CrossRef][ISI]
Bullock S. H. 1994 Wind pollination of neotropical dioecious trees. Biotropica 26: 172-179[CrossRef][ISI]
Charlesworth B. D. Charlesworth 1978 A model for the evolution of dioecy and gynodioecy. American Naturalist 112: 975-997[CrossRef][ISI]
Charlesworth D. 1984 Androdioecy and the evolution of dioecy. Biological Journal of the Linnean Society 23: 333-348
Cook O. F. 1903a Four new species of the Central American rubber tree. Science, New series 18: 436-439
Cook O. F. 1903b The culture of the Central American rubber tree. Goverment Printing Office, Washington, D.C., USA
Corner E. J. H. 1962 The classification of Moraceae. Gardens' Bulletin Singapore 19: 187-252
Dommée B. A. Geslot J. D. Thompson M. Reille N. Denelle 1999 Andromonoecy in the entomophilous tree Fraxinus ornus (Oleaceae). New Phytologist 143: 419-426[CrossRef][ISI]
Endress P. K. 1994 Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge, UK
Fritsch P. L. H. Rieseberg 1992 High outcrossing rates maintain male and hermaphrodite individuals in populations of the flowering plant Datisca glomerata. Nature 359: 633-636[CrossRef]
Hammel B. E. 1986 The vascular flora of La Selva Biological Station, Costa Rica, Moraceae. Selbyana 9: 243-259
Herre E. A. C. A. Machado J. Nason D. M. Windsor S. S. McCafferty W. Van Houtten K. Bachmann 1996 Molecular phylogenies of figs and their pollinator wasos. Journal of Biogeography 23: 521-530[CrossRef][ISI]
Hiura T. K. Ishida 1994 Reproductive ecology in Fraxinus lanuginosa. I. breeding structure. Transactions of the Hokkaido Branch of the Japanese Forest Society 42: 58-60 (in Japanese)
Humphries C. J. S. Blackmore 1989 A review of the classification of the Moraceae. In P. R. Crane and S. Blackmore [eds.], Evolution, systematics, and fossil history of the Hammamelidae, vol. 2, 267–277. Clarendon Press, Oxford, UK
Ishida K. T. Hiura 1998 Pollen fertility and flowering phenology in an androecious tree, Fraxinus lanuginosa (Oleaceae), in Hokkaido, Japan. International Journal of Plant Sciences 159: 941-947[CrossRef]
Janzen D. H. 1979 How to be a fig. Annual Review of Ecology and Systematics 10: 13-51
Kevan P. G. H. G. Baker 1983 Insect as flower visitors and pollinators. Annual Review of Entomology 28: 407-453[CrossRef][ISI]
Kirk W. D. J. 1984 Pollen feeding in thrips (Insecta: Thysanoptera). Journal of Zoology 204: 107-117
Kirk W. D. J. 1985 Effects of some floral scents on host finding by thrips (Insecta: Thysanoptera). Journal of Chemical Ecology 11: 35-43
Lepart J. B. Dommée 1992 Is Phillyrea angustifolia L. (Oleaceae) an androdioecious species?. Botanical Journal of the Linnean Society 108: 375-387
Lewis T. 1973 Thrips: their biology, ecology and economic importance. Academic Press, New York, New York, USA
Liston A. L. L. H. Riesberg T. S. Elias 1989 Datisca glomerata is functionally androdioecious. Nature 343: 641-642
Lloyd D. G. 1975 The maintenance of gynodioecy and androdioedy in angiosperms. Genetica 45: 325-339[CrossRef][ISI]
Mayer S. S. D. Charlesworth 1991 Cryptic dioecy in flowering plants. Trends in Evolution and Ecology 6: 320-325
Molau U. H. Prentice 1992 Reproductive system and population structure in three arctive Saxifraga species. Journal of Ecology 80: 149-161[CrossRef]
Momose K. A. Hatada R. Yamaoka T. Inoue 1998 Pollination biology of the genus Artocarpus, Moraceae. Tropics 7: 165-172
Momose K. T. Nagamitsu T. Inoue 1998 Thrips cross-pollination of Popowia pisocarpa (Annonaceae) in a lowland dipterocarp forest in Sarawak. Biotropica 30: 444-448[CrossRef][ISI]
Mound L. A. R. Marullo 1996 The thrips of Central and South America: an introduction (Insecta: Thysanoptera). Associated Publishers, Gainesville, Florida, USA
Mound L. A. J. M. Palmer 1992 Thrips of Panama: a biological catalogue and bibliography (Thysanoptera). In D. Quintero and A. Aiello [eds.], Insects of Panama and Mesoamerica, selected studies, 321–328. Oxford Univeristy Press, Oxford, UK
Mound L. A. I. Terry 2001 Thrips pollination of the central Australian Macrozamia macdonnellii (Cycadales). International Journal of Plant Sciences 162: 147–154 [CrossRef]
Muenchow G. E. 1998 Subandrodioecy and male fitness in Sagittaria lancifolia subsp. lancifolia (Alismataceae). American Journal of Botany 85: 513-520[Abstract]
Norton S. A. 1984 Thrips pollination in the lowland forest of New Zealand. New Zealand Journal of Ecology 7: 157-164
Ornduff R. 1964 The breeding system of Oxalis suksdorfii. American Journal of Botany 51: 307-314[CrossRef][ISI]
Ornduff R. 1972 The breakdown of trimorphic incompatibility in Oxalis section Corniculatae. Evolution 26: 52-65[CrossRef][ISI]
Pannell J. 1997 Variation in sex ratios and sex allocation in androdioecious Mercurialis annua. Journal of Ecology 85: 57-69[CrossRef]
Parker G. G. A. P. Smith K. P. Hogan 1992 Access to the upper forest canopy with a large tower crane. BioScience 42: 664-670[CrossRef][ISI]
Pellmyr O. L. B. Thien G. Bergstorm I. Groth 1990 Pollination of New Caledonian Winteraceae: opportunistic shifts or parallel radiation with their pollinators?. Plant Systematics and Evolution 173: 143-157[CrossRef][ISI]
Pellmyr O. J. N. Thompson 1992 Multiple occurrences of mutualism in the yucca moth lineage. Proceedings of the National Academy of Sciences, USA 89: 2927-2929
Pellmyr O. J. N. Thompson J. Brown R. G. Harrison 1996 Evolution of pollination and mutualism in the yucca moth lineage. American Naturalist 148: 827-847[CrossRef][ISI]
Philbrick C. T. L. H. Rieseberg 1994 Pollen production in the androecious Datisca glomerata (Datiscaceae): implications for breeding system equilibrium. Plant Species Biology 9: 43-46[CrossRef]
Pittier H. 1910 A preliminary treatment of the genus Castilla. Contributions from the United States National Herbarium 13: 247-249
Rieseberg L. H. C. T. Philbrick P. E. Pack M. A. Hason P. Firtsch 1993 Inbreeding depression in androdioecious populations of Datisca glomerata (Datiscaceae). American Journal of Botany 80: 757-762[CrossRef][ISI]
Rohwer J. G. 1993 Moraceae. In K. Kubitzki, J. G. Rohwer, and V. Bittrich [eds.], Flowering plants, dicotyledons: magnoliid, hamamelid and caryophyllid families, 438–453. Springer Verlag, Heidelberg, Germany
Rust R. W. 1980 Pollen movement and reproduction in Arisaema triphyllum. Bulletin of the Torrey Botanical Club 107: 539-542[CrossRef][ISI]
Sakai S. M. Kato H. Nagamasu 2000 Artocarpus (Moraceae)–gall midge pollination mutualism mediated by a male-flower parasitic fungus. American Journal of Botany 87: 440-445
SAS. 1988 SAS/STAT user's guide. Statistics, version 6. SAS Institute, Cary, North Carolina, USA
Swensen S. M. J. N. Luthi L. H. Rieseberg 1998 Datiscaceae revised: monophyly and the sequence of breeding system evolution. Systematic Botany 23: 157-169
Thien L. B. 1980 Patterns of pollination in the primitive angiosperms. Biotropica 12: 1-13
Thomson J. D. K. R. Shivanna J. Kendrick R. B. Knox 1989 Sex expression, breeding system, and pollen biology of Ricinocarpos pinifolius: a case of androdioecy?. American Journal of Botany 76: 1048-1059[CrossRef][ISI]
Triapitsyn S. V. D. H. Headrick 1995 A review of the Nearctic species of the thrips-attacking genus Ceranisus Walker (Hymenoptera: Eulophidae). Transactions of the American Entomological Society Philadelphia. 121: 227-248
Valiente-banuet A. A. Rojas-martÍnez M. C. Arizmendi P. Dávila 1997 Pollination biology of two columnar cacti (Neobuxbaumia mezcalaensis and Neobuxbaumia macrocephala) in the Tehuacan Valley, Central Mexico. American Journal of Botany 84: 452-455[Abstract]
Webber A. C. G. Gottsberger 1995 Floral biology and pollination of Bocageopsis multiflora and Oxandra euneura in Central Amazonia, with remarks on the evolution of stamens in Annonaceae. Feddes Repertorium 106: 515-524
Wiebes J. T. 1979 Coevolution of figs and their insect pollinators. Annual Review of Ecology and Systematics 10: 1-12
Williams G. P. Adam 1993 Ballistic pollen release in Australian members of Moraceae. Biotropica 25: 478-480[CrossRef][ISI]
Yamazaki T. 1993 Tribe 4: Fraxineae. In K. Iwatsuki, T. Yamazaki, D. E. Boufford, and H. Ohba [eds.], Flora of Japan, vol. IIIa (Angiospermae, Dicotyledoneae, Sympetalae [a]). Kodansha, Tokyo, Japan (in Japanese)
Zapata T. R. M. T. K. Arroyo 1978 Plant reproductive ecology of a secondary deciduous tropical forest in Venezuela. Biotropica 10: 221-230
This article has been cited by other articles:
|
|
 |
|
  M. Mackiewicz, A. Tatarenkov, D. S. Taylor, B. J. Turner, and J. C. Avise Extensive outcrossing and androdioecy in a vertebrate species that otherwise reproduces as a self-fertilizing hermaphrodite PNAS, June 27, 2006; 103(26): 9924 - 9928. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. L. Datwyler and G. D. Weiblen On the origin of the fig: phylogenetic relationships of Moraceae from ndhF sequences Am. J. Botany, May 1, 2004; 91(5): 767 - 777. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Sakai Aristolochia spp. (Aristolochiaceae) pollinated by flies breeding on decomposing flowers in Panama Am. J. Botany, March 1, 2002; 89(3): 527 - 534. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
