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1 Harvard University Herbaria, Cambridge, Massachusetts 02138; and 2 Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak, Malaysia
Received for publication December 3, 1998. Accepted for publication April 22, 1999.
ABSTRACT
Reproductive traits of tropical tree species vary predictably in relation to successional stage, but this variation may be due to the species' phylogenetic histories rather than selective pressures imposed by regeneration requirements. Reproductive phenology, tree size at the onset of reproduction, and fecundity of 11 sympatric, closely related Macaranga species were studied to investigate within-species variation in reproductive traits in relation to resource availability, and among-species variation in relation to other life-history traits (shade tolerance, seed size and maximum tree size, Hmax) and consequently the requirements for forest-gap colonization. Nine species reproduced in synchronous episodes, and two species reproduced continuously over 32 mo. Episodic reproduction was most intense in 1992 following a severe drought. For several species, reproductive trees had greater light availability, lower fecundity in lower light levels, and lower growth rates than nonreproductive trees, reflecting resource-limited reproduction. Among species, Hmax was negatively correlated with shade tolerance and seed size. Tree size at the onset of reproduction and fecundity was strongly linked to this axis of life-history variation, but phenological pattern was not. Absolute tree size at the onset of reproduction was positively correlated with Hmax and negatively correlated with shade tolerance. Relative size at reproductive onset was not correlated with shade tolerance or Hmax. Fecundity ranged four orders of magnitude among species and was correlated positively with Hmax and negatively with seed size and shade tolerance. The interrelationships among these reproductive and other life-history traits are strongly correlated with the species' requirements for gap colonization.
Key Words: early-successional trees • Euphorbiaceae • Macaranga • Malaysia • onset of reproduction • seed size • shade tolerance • succession • tree height • tropical rain forest
The reproductive traits of tropical rain forest trees are usually considered to vary predictably in relation to the time that species appear in forest succession after disturbance (Bazzaz and Pickett, 1980
; Whitmore, 1983
; Denslow, 1987
; Schupp et al., 1989
). For example, pioneer species are often characterized as having early and frequent flowering and the copious production of small and easily dispersed seeds (Swaine and Whitmore, 1988
). However, studies of pioneer species have found a wide range of variation in reproductive traits that may influence the ability of the species to colonize spatially and temporally unpredictable forest gaps. Flowering phenology (Opler, Baker, and Frankie, 1975
; Lambert and Marshall, 1991
; Milton, 1991
), seed size (Fleming et al., 1985
; Foster and Janson, 1985
; Metcalfe and Grubb, 1995
; Grubb, 1996
), dispersal modes (Augspurger, 1986
; Augspurger and Franson, 1988
), dormancy (Dalling, Swaine, and Garwood, 1997
), and fecundity (Fleming, 1985
; Alvarez-Buylla and Martinez-Ramos, 1992
) vary substantially among pioneer trees. This is not surprising since pioneer species have evolved in a wide range of tropical tree lineages, and variation in their functional characteristics may in part depend on the characteristics of the lineage from which species evolved (Kochmer and Handel, 1986
; Harvey and Pagel, 1991
; Wright and Calderon, 1995
). Furthermore, no single functional trait defines any grouping of tropical rain forest trees; pioneer species vary in a wide range of ecophysiological and demographic traits, yet many species successfully colonize and co-occur in forest gaps (Ackerly, 1996
; Strauss-Debenedetti and Bazzaz, 1996
; Davies, 1998
).
A suite of interrelated traits enables species to colonize particular microsites, but may simultaneously limit their ability to colonize and survive in other sites. For example, the production of large, well-defended seeds may inevitably result in a reduction in fecundity (Fleming, 1981
; Grubb, 1998
) and hence reduced ability to colonize spatially scattered and ephemeral forest gaps. Studies of factors influencing the ability of tropical pioneer trees to colonize forest gaps have often focused on either individual species or individual reproductive traits (e.g., Foster and Janson, 1985
; Alvarez-Buylla and Martinez-Ramos, 1992
). However, this approach does not provide a basis to investigate potential trade-offs in reproductive traits among tropical tree species and may not account for the importance of phylogeny in influencing the reproductive life-history traits of species (Barrett, Harder and Worley, 1996
).
In this study, we use a comparative approach to investigate variation in patterns of reproductive onset, phenology, and fecundity among 11 sympatric species of Macaranga (Euphorbiaceae) in Borneo. The species range from very high-light demanding to moderately shade-tolerant trees (Davies, 1998
; Davies et al., 1998
) and vary in other life-history traits such as maximum tree size and seed mass. We test the hypothesis that the more high-light demanding Macaranga species have earlier and more frequent reproduction and greater fecundity than the more shade-tolerant species. First, we test for significant differences in tree size at the onset of reproduction, phenology, and fecundity among the species and assess possible environmental and allocational causes of within-species variation in reproductive activity. We then investigate the interrelationships among reproductive and other life-history traits for the species. In general, fecundity may be positively correlated with maximum tree size among species due to architectural and allocational constraints on seed production, however, seed size variation and the requirements for high-light microsites may affect this relationship (Fleming, 1985
). We investigate potential trade-offs among reproductive and life-history characteristics in relation to differences in microsite preferences among the species. We also consider how this range of life-history traits influences the coexistence of this diverse group of sympatric, closely related species.
MATERIALS AND METHODS
Study species
Macaranga includes ~300 species of tropical trees distributed between west Africa and the south Pacific Islands (Whitmore, 1981
). In Borneo there are ~50 species, many of which are high-light demanding pioneer trees. Eleven sympatric pioneer Macaranga species, in or closely related to section Pachystemon, were chosen for this study (Table 1). All Bornean species of Macaranga are dioecious. In the species included in this study, leaves are clustered toward the ends of orthotropic shoots and the inflorescences, borne in each of the leaf axils, are either developed with or just below the leaves (here referred to as "reproductive shoot clusters"). Staminate inflorescences are panicles with tiny (~0.5–1 mm) apetalous flowers. Small clusters of 5–25 flowers are subtended by green or pale-brown small leafy bracteoles that are sometimes glandular. Pistillate inflorescences differ from staminate inflorescences in being stouter, less branched, and with fewer flowers. The mechanism of insect attraction to the pistillate flowers is unknown. Pistillate flowers are apetalous, 2–6 carpellate, with a single ovule per carpel, and with prominent stigmas that protrude from the calyx. Inflorescences are commonly visited by trigonid bees and thrips (Taylor, 1982
; Momose et al., 1998
), although how pollination occurs is unclear. Pollen is dehisced through the apex of the tubular calyx and collects in and around the flower clusters. The fruits dehisce at maturity exposing small (1–6 mm diameter, 2–64 mg), arillate seeds that are dispersed by a wide variety of small birds and mammals (Taylor, 1982
; Mitchell, 1994
; Davies, personal observation).
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). Daily mean maximum temperatures are ~32°C. The vegetation of Lambir is lowland mixed dipterocarp rain forest of exceptional tree species diversity (LaFrankie, Tan, and Ashton, 1995
; Davies and Becker, 1996
).
The phenological study involved monitoring 1191 trees in two noncontiguous 4-ha subplots of a recently established 52-ha long-term ecological research plot and in seven smaller forest plots in Lambir National Park over ~32 mo, from November 1991 to August 1994. All Macaranga trees in each plot were visited approximately once every 5 wk and scored as reproductive or not. Since pistillate flowers are apetalous and there is no externally obvious distinction between flowering and fruiting stages of reproduction, description of pistillate phenological patterns in this paper includes anthesis to fruit set. Trees across all size classes were monitored to enable estimates of species' size at the onset of reproduction, using both the size of the smallest reproductive individual and the size threshold above which the majority of individuals reproduce. The reproductive size threshold (RST) was estimated for the heavy flowering period in 1992, using the logistic regression model of Thomas (1996b)
. Occasional censuses were missed; for analysis, missed censuses for a tree were counted as reproductive if the census periods on either side of the missed census were both scored as reproductive. For M. havilandii, four censuses were missed in the middle of the survey period, and analyses did not include this period for this species.
Fecundity was estimated for all reproductive trees in the plots, as well as for extra trees of less common species from outside the plots. Counts were made of the total number of reproductive shoot clusters on each tree, and the number of inflorescences on five (or all if there were fewer than five) reproductive shoot clusters. Flower number and seed production per inflorescence were counted on one inflorescence or infructescence from 3–12 different trees for each species. Fecundity for each tree was then estimated as the product of the number of reproductive shoot clusters, the mean number of inflorescences per reproductive shoot cluster, and the mean number of flowers/seeds per inflorescence/infructescence.
For analysis of within-species variation in reproductive traits, individual tree diameters at the time of reproductive activity were interpolated based on individual growth rates over the 32-mo study period (Davies, unpublished data). Tree canopy light environment was assessed using a crown illumination (CI) index on a scale of 5 (high-light) to 1 (low light), following Clark and Clark (1992)
, and calibrated against hemispherical fish-eye photographs (see Davies et al., 1998
). Mean CI index, based on a large number of individuals for each species, is used as an ecological estimate of species' shade tolerance (5, very intolerant to 1, shade tolerant). Maximum tree size (Hmax) was estimated as asymptotic maximum height following Thomas (1996a)
, and described fully in Davies et al. (1998)
. Standard nonparametric tests were used for statistical comparisons of growth between reproductive and nonreproductive trees, because of the nonnormality of these data (Sokal and Rohlf, 1981
).
Phenology analysis
Phenological patterns of reproductive activity were analyzed using circular statistics (Batschelet, 1981
; Milton, 1991
). The dates of phenological events were converted to angles between 0° and 360°. The mean angle, 
, and vector length, r, were then calculated as:
). Reproductive phenology was analyzed at both individual and population levels for each species for 1992 and 1993, and for the sexes separately. For each reproductive individual, the mean angle and vector length were calculated. For each species, individual vector lengths were averaged (rind). rind indicates the average degree of individual temporal aggregation of reproductive activity, for example, a high rind indicates that individuals typically reproduce for a short period at one time of the year even though the date may differ among individuals (assuming no bimodality); alternatively a small rind indicates that individuals typically reproduce in a larger proportion of censuses in one or more episodes. At the population level, the mean angles for all individuals of a species were then analyzed together, resulting in a population vector length (rpop) and mean angle. The mean angle for the population indicates the average date of peak reproductive activity among the individuals. rpop indicates the degree of among-individual aggregation or synchrony of reproductive activity.
RESULTS
Size at reproductive onset
Tree size at the onset of reproduction varied dramatically among the 11 Macaranga species (Table 1). Reproductive size threshold (RST) ranged from 1.1 (M. havilandii) to 18.8 (M. hosei) cm dbh (diameter at breast height), and the minimum reproductive size observed (Rmin) ranged from 0.6 to 9.7 cm dbh. Among species, RST was 24–44% of Hmax, and Rmin was 9–32% of Hmax. RST for M. hosei was probably an overestimate as reproductive trees of 10–12 cm dbh were frequently observed outside the study plots (Davies, personal observation). There were no significant between-sex differences in size at the onset of reproduction (Kolmogorov-Smirnov two-sample tests, P > 0.2 for all species).
Reproductive phenology
Nine of the 11 Macaranga species (M. gigantea, M. hosei, M. hypoleuca, M. triloba, M. beccariana, M. trachyphylla, M. hullettii, M. lamellata, and M. kingii) reproduced in synchronous episodes twice during the study period ("episodic"), with a third episode starting as the study was terminated in 1994 (Fig. 1). Large population vector lengths, rpop, in these species (range: 0.59–1.00, mean: 0.92, N = 30, with years and sexes separate; Table 2) indicated a high degree of intraspecific reproductive synchrony, and high means of the individual vector lengths, rind (range: 0.68–1.00, mean: 0.93, N = 30), reflected relatively short reproductive duration. In contrast, M. winkleri and M. havilandii reproduced continuously at the population level throughout the study period ("continuous"), although several censuses were missed for M. havilandii (Fig. 1). rpop values were lower (range: 0.28–0.77, mean: 0.55, N = 6), indicating less synchronized within-species reproduction. rind values were also lower, as individuals reproduced in a large proportion of months (range: 0.20–0.69, mean: 0.47, N = 6; Table 2).
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Reproductive frequency varied within all species (Table 3). Trees of episodic species reproduced up to three times, yet 21–68% of trees > Rmin (0–25% of trees > RST) did not reproduce during the study period. In several species (M. beccariana, M. trachyphylla, and M. kingii) pistillate trees tended to flower more frequently than staminate trees (Table 3). Individual trees of both continuous species were reproductive for, on average, 49–66% of the censuses, with no differences between the sexes (Table 4). Although some trees were reproductively active throughout the 32-mo period, 17–37% of trees with dbh > RST failed to reproduce.
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Fecundity
Flower and fruit production varied enormously among Macaranga species (Fig. 3). Trees produced from 103 (M. havilandii) to 107 (M. gigantea, M. hosei, M. hypoleuca, and M. winkleri) staminate flowers or from 102 to >105 seeds per reproductive episode. For continuous reproducers, annual fecundity was approximately three times the values for a single reproductive episode (Davies, personal observation). Species differed significantly in the production of both inflorescences per tree and flowers per inflorescence (Table 5). Differences in staminate and pistillate fecundity were primarily due to differences in flowers per inflorescence; inflorescence production per tree did not differ significantly between the sexes in any species.
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Reproduction and other life-history traits
All measures of phenological pattern (rind, rpop, reproductive frequency, and mean date of reproduction) among the 11 Macaranga species were not significantly correlated with other reproductive traits (tree size at the onset of reproduction or fecundity) or with other life-history traits (Hmax, estimated shade tolerance, or seed mass) (P > 0.05 in all cases). In contrast, tree size at the onset of reproduction and mean annual fecundity were strongly correlated with other life-history traits. Tree size at the onset of reproduction was positively correlated with Hmax (RST: rs = 0.91, Rmin: rs = 0.85, both P < 0.01), negatively correlated with seed mass (rs = -0.66, P = 0.04), and positively correlated with species' mean CI index (for RST, rs = 0.77, P = 0.01) and therefore negatively correlated with estimated shade tolerance. However, relative size at the onset of reproduction was not significantly correlated with Hmax, seed mass, or estimated shade tolerance (all P > 0.1). Among species, mean annual fecundity was positively correlated with Hmax and negatively correlated with shade tolerance and seed mass (Fig. 3). The mean number of inflorescences per tree (
: rs = 0.77, 
: rs = 0.88) and the mean number of flowers per inflorescence (: rs = 0.91, : rs = 0.79) were significantly positively correlated with Hmax (all P < 0.02). The number of pistillate flowers per inflorescence was negatively correlated with mean seed size (rs = -0.87).
DISCUSSION
The phenological patterns found in the 11 Macaranga species are consistent with patterns reported for Macaranga elsewhere in southeast Asia (Taylor, 1982
; van Schaik, 1986
; Corlett, 1990
). The 5-wk census interval used and the difficulty of identifying the exact flowering time in pistillate plants may limit our ability to detect finer scale temporal differences in flowering activity, particularly among the episodic species. However, field observations suggested that flowering was concurrent among species, as anthesis occurs acropetally within and among inflorescences on a reproductive shoot, and inflorescences expand over 3–6 wk (Davies, personal observation). When closely related species are truly sympatric, they often flower at different times or have different flower morphologies and pollinators (Hurlbert, 1970
; Stiles, 1975
; Fleming, 1985
; Ashton, Givnish, and Appanah, 1988
; Yap and Chan, 1990
; LaFrankie and Chan, 1991
; Oliveira and Gibbs, 1994
; but see Wright and Calderon, 1995
). In these species of Macaranga flower morphologies are uniform, and species appear to share pollinators. Whether there are detrimental consequences to this apparent phenological overlap (Bawa, 1983
) and what the reproductive isolating mechanisms in these species are require detailed study of pollinator visitation patterns, flower anthesis, and fruit maturation (Augspurger, 1981
).
Community-level reproduction was synchronized, but not strictly annual among the nine episodic Macaranga species, suggesting that they responded to a common flowering cue. In 1992, the heaviest flowering year, there was an intense short-term drought at Lambir between January and March (Fig. 1), with cumulative 30-d rainfall <40 mm for 39 d. A general flowering of Dipterocarpaceae and other canopy species followed the drought (Davies, personal observation). The slightly later and less intense Macaranga flowering in 1993 was not preceded by an intense drought; cumulative 30-d rainfall from January to March was <40 mm for only 14 d. In 1994, flowering was initiated (although intensity was not assessed) even though cumulative rainfall in the same period was >170 mm. Our observations from 1992 to 1998 indicate that these species reproduce in all years, with considerable variation in the intensity of reproduction; species reproduce most heavily in the same years as forest-wide general flowering (see also Sakai et al., 1999
). This variation may be linked to increased irradiance levels associated with drought periods as suggested by other workers (van Schaik, Terborgh, and Wright, 1993
; Wright and van Schaik, 1994
).
A large proportion of mature trees of most Macaranga species did not reproduce during the study, and there was significant variation in reproductive frequency. Much of this variation may have been due to variation in resource availability. Diameter growth in these species was shown to be strongly limited by light and soil resource availability (Davies, unpublished data). Reproductive trees in most species had their canopies in higher light levels than nonreproductive trees, and several species had greater reproductive frequency in higher light or reduced pistillate fecundity in lower light, suggesting that reproduction was strongly influenced by resource availability. Fecundity in pistillate plants may have been particularly sensitive to resource limitation, as tree size accounted for less of the variation in pistillate than staminate fecundity in most species (see also Melampy and Howe, 1977
; Bullock and Bawa, 1981
; Bullock, 1982
; Bullock, Beach, and Bawa, 1983
; Clark and Clark, 1987
; Armstrong and Irvine, 1989
; Thomas and LaFrankie, 1993
; Thomas, 1996c
). However, pistillate trees in several species flowered more frequently than staminate trees. A consequence of resource-limited reproduction may be reduced growth rates in reproductive trees (Bazzaz and Reekie, 1985
). Reproductive trees had lower diameter growth rates in two species, and for M. winkleri reproductive frequency was negatively correlated with growth rate. However, if reproductive and nonreproductive trees are differentially distributed on a fine scale with respect to resource availability, reproductive trees may grow as fast or faster than nonreproductive trees. For M. triloba, growth rates were higher in reproductive than nonreproductive trees, but nonreproductive trees of this species were in particularly unfavorable microsites, their canopies had much lower light levels (Fig. 2), and they had higher mortality rates (Davies, 1996
).
Reproduction and life history
Reproductive phenology was not correlated with other life-history traits among the 11 Macaranga species. The continuous reproducers, M. winkleri and M. havilandii, have extremely different life histories (Davies, 1998
; Davies, unpublished data). Macaranga winkleri is a high-light-demanding tree of 15–20 m tall, restricted to nutrient-rich soils. Trees grow rapidly to reproductive maturity, produce a huge number of tiny seeds, incurring an indirect cost in reduced growth rates, and then continue to reproduce for several years before dying. Macaranga havilandii is relatively shade tolerant and occurs on nutrient-poor soils often associated with small landslips. It grows slowly to 5–6 m tall and produces a small number of relatively large seeds. Continuous seed production in M. havilandii may ensure seed availability in the unpredictable event of a small landslip, in which seed would not be available in the soil. The episodic species also vary in life-history traits, with species ranging from relatively shade tolerant (e.g., M. kingii) to very high-light-demanding (e.g., M. gigantea), and differing in fecundity, Hmax, and seed size (Davies et al., 1998
).
Pioneer tree species are usually considered to initiate reproduction earlier than shade-tolerant species (Bazzaz, 1984
; Swaine and Whitmore, 1988
). Given that pioneers typically access higher resource levels and grow faster, they not surprisingly reach reproductive size sooner than other species. However, we found no evidence for a relationship between successional status and relative size at the onset of reproduction among the 11 Macaranga species. Furthermore, Thomas (1996b)
reported a range of 20–75% for the relative size at the onset of reproduction among 36 shade-tolerant tree species in a peninsular Malaysian rain forest. These values completely overlap the Macaranga values and suggest that the life history of pioneer species, although accelerated, shows no consistent differences from nonpioneer species with regard to relative tree size at the onset of reproduction (see also Brzeziecki and Kienast, 1994
, for temperate trees).
Greater fecundity in more high-light-demanding than shade-tolerant species conforms to the general expectation for tropical trees (Swaine and Whitmore, 1988
; Primack and Lee, 1991
). However, the more high-light demanding species were also larger trees and produced smaller seeds, so differences in fecundity may or may not represent relative differences in biomass allocation to reproduction. Among Macaranga species, tree size determined the potential number of sites for inflorescence production as was found for the Neotropical pioneer, Cecropia obtusifolia (Alvarez-Buylla and Martinez-Ramos, 1992
). Larger Macaranga species also had more elaborately branched inflorescences bearing more flowers. The direct reason for this is unclear, but seed size was negatively correlated with the number of pistillate flowers per inflorescence and may constrain potential flower production per inflorescence. The selective advantage of smaller seeds in more high-light-demanding Macaranga species may be related to a range of factors, including increased dispersal ability to access high-light microsites, lower unit energy costs, and in M. winkleri, the species with the smallest seed, the ability to continuously reproduce and thereby increase the probability of accessing ephemeral gaps (Dalling, Swaine and Garwood, 1997
). Smaller seeds may also have lower seed reserves, may be physically impeded by dense leaf litter, and may have lower persistence times in the soil due to pathogen or drought effects, thereby excluding species from establishment in light-limited microsites (Hopkins and Graham, 1987
; Alvarez-Buylla and Martinez-Ramos, 1990
; Molofsky and Augspurger, 1992
; Grubb, 1998
).
An axis of life-history variation among the 11 sympatric Macaranga species ranges from very high-light-demanding to moderately shade tolerant. Maximum tree size, seed size, absolute tree size at the onset of reproduction, and annual fecundity covary with the degree of shade tolerance in these species. Smaller seeds and greater fecundity may have selective advantages for more high-light-demanding species, however these traits are also strongly correlated with, and may functionally depend upon, tree size and inflorescence architecture. Assessing whether these traits have undergone correlated evolutionary changes associated with the diversification of Macaranga in early-successional environments will be clarified with an explicit hypothesis of phylogenetic relationships.
FOOTNOTES
1 The authors thank the Government of Sarawak, and the Sarawak National Parks and Forest Departments for permission to work at Lambir. The 52-ha Long Term Ecological Research plot was established as a collaborative project of the Sarawak Forest Department, Malaysia, Harvard University, USA (NSF award DEB 9107247 to PSA) and Osaka City University, Japan. The staff of the Sarawak Forest Department and the people of Rumah Ajai Longhouse greatly assisted with the field work. SJD was supported by a graduate student fellowship from the Department of Organismic and Evolutionary Biology and a Deland Award to the Arnold Arboretum at Harvard University. Sean Thomas, Peter Wayne, Fakhri Bazzaz, Tristram Seidler, Peter Stevens and Joe Wright made constructive comments on early versions of the paper. 
2 Author for correspondence: Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia. (e-mail correspondence: sjdavies{at}mailhost.unimas.my
).
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Rmin) in eight Macaranga species. Species listed by their first three letters (see 
0.01 in all cases). Three species were excluded from analyses due to limited sample sizes