American Journal of Botany 86(12): 1786±1795. 1999.

PHENOLOGY AND FECUNDITY IN 11 SYMPATRIC PIONEER SPECIES OF MACARANGA (EUPHORBIACEAE) IN BORNEO1

STUART J. DAVIES2,3,4 AND PETER S. ASHTON2

2Harvard University Herbaria, Cambridge, Massachusetts 02138; and 3Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak, Malaysia

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 nonre-

productive trees, re¯ecting resource-limited reproduction. Among species, Hmax was negatively correlated with shade toler- ance 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 Augspurger and Franson, 1988), dormancy (Dalling, usually considered to vary predictably in relation to the Swaine, and Garwood, 1997), and fecundity (Fleming, time that species appear in forest succession after distur- 1985; Alvarez-Buylla and Martinez-Ramos, 1992) vary bance (Bazzaz and Pickett, 1980; Whitmore, 1983; Den- substantially among pioneer trees. This is not surprising slow, 1987; Schupp et al., 1989). For example, pioneer since pioneer species have evolved in a wide range of species are often characterized as having early and fre- tropical tree lineages, and variation in their functional quent ¯owering and the copious production of small and characteristics may in part depend on the characteristics easily dispersed seeds (Swaine and Whitmore, 1988). of the lineage from which species evolved (Kochmer and However, studies of pioneer species have found a wide Handel, 1986; Harvey and Pagel, 1991; Wright and Cald- range of variation in reproductive traits that may in¯u- eron, 1995). Furthermore, no single functional trait de- ence the ability of the species to colonize spatially and ®nes any grouping of tropical rain forest trees; pioneer temporally unpredictable forest gaps. Flowering phenol- species vary in a wide range of ecophysiological and de- ogy (Opler, Baker, and Frankie, 1975; Lambert and Mar- mographic traits, yet many species successfully colonize shall, 1991; Milton, 1991), seed size (Fleming et al., and co-occur in forest gaps (Ackerly, 1996; Strauss-De- 1985; Foster and Janson, 1985; Metcalfe and Grubb, benedetti and Bazzaz, 1996; Davies, 1998). 1995; Grubb, 1996), dispersal modes (Augspurger, 1986; 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 exam- 1 Manuscript received 3 December 1998; revision accepted 22 April 1999. ple, the production of large, well-defended seeds may The authors thank the Government of Sarawak, and the Sarawak inevitably result in a reduction in fecundity (Fleming, National Parks and Forest Departments for permission to work at Lam- 1981; Grubb, 1998) and hence reduced ability to colonize bir. The 52-ha Long Term Ecological Research plot was established as spatially scattered and ephemeral forest gaps. Studies of a collaborative project of the Sarawak Forest Department, Malaysia, factors in¯uencing the ability of tropical pioneer trees to Harvard University, USA (NSF award DEB 9107247 to PSA) and Osa- ka City University, Japan. The staff of the Sarawak Forest Department colonize forest gaps have often focused on either individ- and the people of Rumah Ajai Longhouse greatly assisted with the ®eld ual species or individual reproductive traits (e.g., Foster work. SJD was supported by a graduate student fellowship from the and Janson, 1985; Alvarez-Buylla and Martinez-Ramos, Department of Organismic and Evolutionary Biology and a Deland 1992). However, this approach does not provide a basis Award to the Arnold Arboretum at Harvard University. Sean Thomas, to investigate potential trade-offs in reproductive traits Peter Wayne, Fakhri Bazzaz, Tristram Seidler, Peter Stevens and Joe among tropical tree species and may not account for the Wright made constructive comments on early versions of the paper. 4 Author for correspondence: Institute of Biodiversity and Environmental importance of phylogeny in in¯uencing the reproductive Conservation, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sa- life-history traits of species (Barrett, Harder and Worley, rawak, Malaysia. (e-mail correspondence: [email protected]). 1996). 1786 December 1999] DAVIES AND ASHTONÐTROPICAL TREE PHENOLOGY AND FECUNDITY 1787

TABLE 1. Life history traits for 11 species of Macaranga. Reproductive size threshold (RST, dbh in cm), and minimum observed reproductive size

(Rmin, dbh in cm) from this paper, and Hmax (estimated maximum tree height), shade tolerance (estimated from mean crown illumination index, where lower values indicate greater tolerance) and seed mass from Davies et al. (1998). Values in parentheses are species' relative reproductive

sizes (as a percentage of maximum tree dbh). Nr is the number of reproductive individuals, Nt is the total sample size. Species arranged as in Fig. 1.

Reproductive size Shade Seed Hmax tolerance mass RST Rmin Macaranga species (m) (mean CI) (mg) (cm, %) (cm, %) Nr Nt Episodic reproduction gigantea (Reichb. f. & Zoll.) Muell. Arg. 29.3 4.2 13.7 12.2 (29) 9.7 (23) 2 38 hosei King ex Hook. f. 31.3 4.0 5.1 18.8 (34) 7.6 (14) 3 104 hypoleuca (Reichb. f. & Zoll.) Muell. Arg. 22.5 3.6 22.4 9.4 (26) 3.8 (11) 5 36 triloba (Bl.) Muell. Arg. 22.4 3.4 17.0 3.6 (24) 1.4 (9) 68 190 beccariana Merr. 17.2 3.4 15.2 5.3 (37) 2.6 (18) 37 255 trachyphylla Airy Shaw 21.5 3.2 22.7 7.3 (31) 4.8 (21) 34 233 hullettii King ex Hook. f. 17.9 2.6 28.3 4.6 (34) 4.4 (32) 13 33 lamellata Whitmore 15.0 2.1 64.0 3.7 (40) 1.2 (13) 13 52 kingii Hook. f. var. platyphylla Airy Shaw 14.9 2.0 64.2 2.2 (30) 1.2 (16) 23 53 Continuous reproduction winkleri Pax & Hoffm. 21.5 4.0 1.7 5.5 (37) 2.8 (19) 33 98 havilandii Airy Shaw 5.6 2.8 23.5 1.1 (44) 0.6 (24) 38 99

In this study, we use a comparative approach to inves- 25 ¯owers are subtended by green or pale-brown small leafy bracteoles tigate variation in patterns of reproductive onset, phenol- that are sometimes glandular. Pistillate in¯orescences differ from sta- ogy, and fecundity among 11 sympatric species of Ma- minate in¯orescences in being stouter, less branched, and with fewer caranga (Euphorbiaceae) in Borneo. The species range ¯owers. The mechanism of insect attraction to the pistillate