Journal of E€ect of light on the germination of forest trees in Ecology 1999, 87, 772±783 Ghana

B. KYEREH*, M. D. SWAINE{ and J. THOMPSON{{ *Institute of Renewable Natural Resources, University of Science and Technology, Kumasi, Ghana; {Department of Plant and Soil Science, University of Aberdeen, Aberdeen AB24 3UU, UK; and {Forestry Research Institute of Ghana, University PO Box 63, Kumasi, Ghana

Summary 1 Seed germination in light and dark, and responses to irradiance and light quality, were tested in shadehouse experiments for 19 West African tropical forest tree spe- cies representing a wide range of ecological types. Germination in forest gaps of di€erent size was tested for 11 species. 2 Percentage germination was reduced in the dark only for three small-seeded spe- cies that are common in forest soil seed banks: Musanga cecropioides, Nauclea diderrichii and Milicia excelsa. Percentage germination of the other 16 species, including four widely regarded as `pioneers', was una€ected. 3 E€ects of di€erent irradiances in shadehouses, where the seeds were watered, were signi®cant for some species, but there was no consistent pattern. Irradiance e€ects in forest gaps, where the seeds received only natural wet season rainfall, were more widespread and substantial, and were most commonly shown as a depression of percentage germination at high irradiance. 4 E€ects of light quality (neutral vs. green shade; red : far-red = 0.43) were insignif- icant at 5% irradiance in shadehouses for all species except Nauclea diderrichii.In growth chamber experiments, the low energy response was only evident at 1.0 mmol m±2 s±1 (< 1% of unshaded forest irradiance) in Musanga and Nauclea. 5 The speed of germination was a€ected by irradiance in many species, but the e€ect was small compared with di€erences between species, in which time to com- plete germination varied between 3 weeks and over 6 months. 6 Seeds of Ceiba pentandra and Pericopsis elata planted in deep forest shade (2% irradiance) and in a small gap (30% irradiance) germinated well in both sites, showed exponential biomass growth in the gap but a linear decline in mean seed- ling biomass and subsequent death in deep shade. 7 Light-mediated germination is relatively rare among these forest trees, even among pioneers, so that the working de®nition of a pioneer should be seen to depend more on a species' ability to survive in forest shade. The e€ects of canopy opening on seed germination are small except in the largest openings, which severely depress germination in a number of species, including some species with strongly light-demanding seedlings.

Key-words: irradiance, photoblastic seeds, pioneers, red : far-red ratio Journal of Ecology (1999) 87, 772±783

Introduction butions have been made by Va zquez-Ya nes and co- workers in Mexico (Va zquez-Yanes 1977, 1980; Environmental in¯uences on the germination of tro- Va zquez-Yanes & Orozco-Segovia 1982a, b, 1984, pical forest species have received much less attention 1990, 1993; Va zquez-Yanes et al. 1990). This may, in than temperate species, although signi®cant contri- part, be due to the perception that most timber tree species from tropical rain forest have recalcitrant

# 1999 British Correspondence: M.D. Swaine (fax 01224 272703; e-mail seeds (sensu Roberts 1973; Corbineau & Comb Ecological Society [email protected]). 1989), which have no dormancy, rapid germination 773 and short viability. With typically high seed moist- able from ®eld experience in any tropical forest B. Kyereh, ure content, recalcitrant seeds are dicult to store, region, but the de®ning characteristics have not M.D. Swaine & but if collected fresh they are easy to germinate and been widely tested by experiment. Raich & Gong J. Thompson establish in nurseries and germinate abundantly in (1990) planted seeds of 43 Malaysian tree species in natural forest. The contrasting seed type, known as forest shade, as well as in small and large canopy orthodox because their seeds can be readily stored gaps, and recorded percentage germination. They in arti®cial conditions, have low seed moisture and recognized three species groups: those that showed generally show various degrees of dormancy. higher germination in gaps, those with higher germi- Recalcitrant seeds are characteristic of non-pioneer nation in forest shade and those that germinated (climax) species, while orthodox seeds are associated well both in shade and in gaps. There were, how- with pioneer species (sensu Swaine & Whitmore ever, no clear discontinuities between the three cate- 1988), which include relatively few timber species gories, and in some cases there were marked (Whitmore 1983). di€erences in response to canopy cover between dif- This dichotomy among tropical forest tree species ferent seed collections of the same species. is a useful generalization, but conceals considerable However, there are several reports of pioneers diversity of species' germination response. Garwood germinating in deep forest shade (e.g. Endospermum (1983), for example, has shown considerable varia- peltatum in Sabah; Kennedy & Swaine 1992). Ceiba tion both between and within species in the period pentandra was observed by M. Dike and D. U. U. of seed dormancy following dispersal, and suggested Okali (personal communication) to germinate in for- that this often allows the seed to germinate at the est shade in Nigeria; and Cecropia spp. were the most favourable season for seedling establishment. most abundant germinants in the understorey of a The speed of germination is also very variable: in Costa Rican rain forest (Li et al. 1996). Such obser- 335 Malaysian tree species, Ng (1980) showed that vations cast doubt on the gap-dependence of pio- the time taken to complete germination varied neers for germination, and thus on the naturalness between 1 week and more than 1 year. of the dichotomy between them and non-pioneers. If Swaine & Whitmore (1988) proposed that tropical this widely recognized and frequently applied forest tree species could be divided into two guilds dichotomy is to be preserved, it becomes more (functional groups; sensu Gitay & Noble 1997), the dependent on the second of the Swaine & Whitmore pioneers and non-pioneers, distinguished by the (1988) criteria for pioneers, the seedling's require- dependence of pioneers on canopy gaps for seed ger- ment for high irradiance. Thus, although pioneers mination and seedling establishment. The implica- may germinate in deep shade, they will usually be tion was that pioneers had seed dormancy that was overlooked and very small seedlings die swiftly in broken by gap conditions (increased irradiance and low irradiance (Kennedy & Swaine 1992). red : far-red ratio, elevated or ¯uctuating tempera- The environmental conditions that break seed tures), associated with a requirement of their seed- dormancy in tropical forest tree seeds may be a high lings for high irradiance, so that the guilds were red : far-red ratio (Va zquez-Ya nes 1977, 1980; naturally distinct. The hypothesis was based on the Orozco-Segovia & Va zquez-Ya nes 1989; Valio & circumstantial evidence that pioneer species were Joly 1979), high maximum temperature or tempera- never found as young seedlings in forest shade, and ture range (Va zquez-Ya nes & Orozco-Segovia only occurred as young plants in canopy gaps or 1982a), ¯uctuating soil moisture (e.g. Terminalia sp.; other disturbed areas such as roadsides and farms. Taylor 1960) or some combination of these. All of Various studies have shown that some pioneer spe- these changes in microclimate can occur following cies require light for germination (photoblasticity) canopy opening, and because they are substantial (Valio & Joly 1979; Va zquez-Yanes & Smith 1982; may also reduce seed germination in non-dormant Orozco-Segovia & Va zquez-Yanes 1989; Va zquez- (non-pioneer) species by causing desiccation or heat- Yanes et al. 1990), which lends support for pioneer ing (insolation). Such environmental e€ects have gap-dependence determined by seed germination. implications for forest management: exploitation of Hawthorne (1993, 1995) provided a subdivision of tropical forest for timber commonly creates large the more speciose non-pioneer guild on the basis of gaps that appear to favour pioneer species over non- seedling ability to survive and grow in deep forest pioneers, because of the di€erential e€ect on seed shade. In such conditions, seedlings of non-pioneer germination and on seedling growth and survival. light demanders (NPLD) have higher mortality, The present study set out to test if West African most dying before exceeding a metre or so in height, pioneer trees have gap-dependent germination as while non-pioneer shade bearers (NPSH) have lower proposed by Swaine & Whitmore (1988), or if their mortality and continue to grow in deep shade, even- failure to establish is due to negative carbon balance # 1999 British tually becoming established trees. in young seedlings. Experimental testing is necessary Ecological Society Journal of Ecology, The pioneer/non-pioneer dichotomy has the because existing allocation to the pioneer guild has 87, 772±783 advantage that the groups are readily distinguish- been based on the subjectively perceived distribution 774 of young plants in forest habitats. We used an has a large and persistent soil seed bank (Hall & Light and experimental approach in shadehouses, growth Swaine 1980) of very small seeds and is an abundant germination of chambers and forest gaps to determine germination colonizer of abandoned farmland in wet forest. forest trees responses to light in West African tree species, cho- Terminalia ivorensis and Terminalia superba are also sen to include both pioneers and a range of non-pio- fast-growing pioneers but achieve larger size and neers as previously categorized by Hall & Swaine their larger seeds (in winged fruits) are uncommon (1981) and Hawthorne (1995). Our strategy was to in soil seed banks. Like Musanga, their seedlings are ®nd out ®rst if the species were photoblastic, in intolerant of shade. Entandrophragma utile has order to determine if further experiments were winged seeds, is absent from soil seed banks (Hall & needed to describe the nature of the light e€ect, and Swaine 1980), and is a non-pioneer light-demander then to examine the e€ect of irradiance on germina- (sensu Hawthorne 1995) somewhat tolerant of shade tion because of its in¯uence on both seed tempera- but growing most rapidly in moderate irradiance. ture and moisture content. The applicability of these Guarea cedrata is an example of the most shade tol- shadehouse results for forest conditions were then erant of West Africa's timber species (a non-pioneer tested by germination trials in arti®cial forest gaps shade-bearer; Hawthorne 1995), with a large seed of of di€erent size. A ®nal experiment compared bio- short viability. Its seedlings are commonly abundant mass accumulation of young seedlings in forest in deep shade, with slow growth, even in non-limit- shade and a canopy gap to test the shade tolerance ing irradiance (Swaine et al. 1997). All species used of seedlings of pioneers. in the study are important timber trees, with the Species nomenclature follows Hawthorne (1995). exception of Musanga which is of small stature and Except where ambiguity may arise, species are has low-density wood. referred to by genus only after the ®rst mention.

SHADEHOUSE EXPERIMENTS

Methods A series of experiments was conducted in seed trays placed in screened shadehouses at the Forestry SPECIES SELECTION Research Institute of Ghana, Kumasi. The shade- A wide range of tree species (Table 1) was chosen houses were constructed for experiments on the for experimental work, representing considerable growth rate of tree seedlings (Agyeman 1994; variation in seed mass (0.3±2940 mg fresh mass) in Swaine et al. 1997) under di€erent degrees of neutral fresh seed moisture content (4±54% fresh mass) and shading provided by bamboo slats (to provide for- ecological guild. The species included the fast-grow- est-like sun¯ecks) and hessian shade cloth, but were ing short-lived pioneer Musanga cecropioides, which also used in the present experiment to provide a

Table 1 Mean mass and mean water content of freshly collected seeds, dispersal morphology and ecological guild of tree species used in germination experiments arranged in order of fresh seed mass. Ecological guilds after Hawthorne (1995): P = pioneer; NPLD = non-pioneer light-demander; NPSH = non-pioneer shade-bearer

Species Code Family Ecological Dispersal Fresh seed Water content guild morphology mass (mg) (% fresh mass)

Blighia sapida Bs Sapind. NPLD Arillate, black seed 2940 46 Ricinodendron heudelotii Rh Euphorbi P Fleshy fruit 1590 10 Pterygota macrocarpa Pm Sterculi. NPLD Winged seed 1466 16 Guarea cedrata Gc Meli. NPSH Fleshy capsule 1021 27 Entandrophragma utile Eu Meli. NPLD Winged seed 595 7 Sterculia rhinopetala Sr Streculi. NPLD Arillate 563 30 Khaya anthotheca Ka Meli. NPLD Winged seed 249 4 Pericopsis elata Pe Papilio. NPLD Winged fruit 220 14 Mansonia altissima Ma Sterculi. NPLD Winged fruit 191 12 Lovoa trichilioides Lt Meli. NPLD Winged seed 186 54 Khaya ivorensis Ki Meli. NPLD Winged seed 165 9 Terminalia ivorensis Ti Combret P Winged fruit 117 10 Terminalia superba Ts Combret P Winged fruit 112 9 Albizia ferruginea Af Mimos. NPLD Winged fruit 105 8 Ceiba pentandra Cp Bombac P Seed in kapok 60 17 Celtis mildbraedii Cm Ulm. NPSH Fleshy fruit 49 14 Funtumia elastica Fe Apocyn. NPLD Plumed seed 34 7 # 1999 British Milicia excelsa Me Mor. P Fleshy fruit 3 7 Ecological Society Musanga cecropioides Mc Mor. P Fleshy fruit 0.8 9 Journal of Ecology, Nauclea diderrichii Nd Rubi. P Fleshy fruit 0.3 7 87, 772±783 775 range of irradiances and for protection from seed were examined only at night with the aid of a dim, B. Kyereh, predators and herbivores. green-®ltered torchlight. A seed was recorded as ger- M.D. Swaine & Kumasi (643 0 N138 0 W) lies in the forest zone of minated once the radicle had emerged. Monitoring J. Thompson Ghana. It has a bimodal rainfall pattern consisting of germination ceased when no further seeds had of a major rainy season (March±July) and a minor germinated for at least 1 week. At this stage, all one (September±November). The mean annual rain- ungerminated seeds appeared decayed, with the fall is about 1500 mm, and the mean annual tem- exception of Ricinodendron. This species has perature is 25.6 C with an average daily range of 8± extended germination and the monitoring period 9 C. Relative humidity at mid-day is lowest in was therefore extended. January, about 47%, and above 85% in the rainy season. Experiments to test for the e€ect of light on ger- GROWTH CHAMBER EXPERIMENTS mination used the 42% irradiance (= 42% of For two of the species that showed a photoblastic unshaded irradiance) shadehouse and shallow woo- response (Musanga and Nauclea) it was thought den seed trays ®lled with forest topsoil and closed necessary to conduct further experiments in con- with a wooden-framed lid that permitted air circula- trolled environment growth chambers at the tion. The lids were covered by two layers of black University of Aberdeen, UK, because of the di- polythene (dark treatment, 0% irradiance), one or culty of controlling temperature in shadehouse con- more layers of clear polythene (neutral shade, to ditions. The Sanyo-Gallenkamp growth chambers give 30% and 5% of unshaded irradiance) or by a were operated at a constant 27 C. Light conditions green ®lter [Strand Lighting, Middlesex, UK, pea- were varied by the use of black or clear polythene, a green ®lter no. 421, reduced red : far-red ratio (0.43), no. 421 pea-green ®lter and another ®lter (Garcia & 5% unshaded irradiance]. Irradiances within the Smith 1993) which provided a lower red : far-red treatment boxes were measured with Didcot ratio light. Combinations of these provided irra- Instruments, Abingdon, Oxford, UK, integrating diances of 0, 0.1, 1, 5 and 30 mmol m±2 s±1, and red : - PAR sensors (DRP2) and expressed as a percentage far-red ratios of 0.83 and 0.43±0.47. Irradiances of the irradiance outside the shadehouse. were measured by integration over 1 week using a Tests of the e€ects of irradiance on a subset of factory-calibrated Skye Instruments, Llandrindod species used 2%, 30% and 65% irradiance shade- Wells, Powys, UK, DataHog. Thirty seeds were houses with open plastic bowls ®lled with forest top- sown on two layers of Whatman no. 1 ®lter paper soil. Shadehouse irradiances were measured in the within Petri dishes in each of four replicates same way as the enclosed germination boxes. Freshly collected fruits and seeds were used in all experiments. These were mostly collected opportu- EXPERIMENTS IN FOREST nistically, so that we did not know how many parent The relevance of the results from the preceding trees were included in each species collection. It is experiments was tested for forest conditions by ger- likely, however, that some collections came from a minating seeds in a range of arti®cial gaps in Tinte single parent. Some collections were made into Bepo Forest Reserve, Ghana, which has a somewhat black plastic bags (e.g. Ceiba, Blighia), but none was drier climate than Kumasi with a mean annual rain- exposed to high irradiance before the experiments. fall of about 1300 mm. Gaps were created by felling As many seeds are exposed on the forest ¯oor after small trees and clearing undergrowth beneath pre- dispersal it is unrealistic to store them in total dark- existing openings in the upper canopy. This method ness. Wings, kapok, pappuses and ¯esh were avoided the felling of large trees. Irradiance in gaps removed from seeds before they were pressed half- was measured by Didcot Instruments integrating way into the soil. Each irradiance treatment was PAR sensors (DRP2). Several sensors were rotated shared among four bowls (to allow randomization among the gaps and there was a ®xed sensor in an on the bench), each with 25 seeds, except for Celtis open area outside the Forest Reserve. Gap size was mildbraedii, for which 20 seeds were used. The adjusted to achieve approximately 15%, 30% and small-seeded species, Musanga, Nauclea diderrichii 50% of unshaded irradiance. Four replicate gaps of and Milicia excelsa (Table 1), received the same each irradiance and four areas of closed canopy for- treatments, but were planted in Petri dishes with est (mean irradiance 2%) were used for the experi- two layers of Whatman no. 1 ®lter paper. The ment, as well as the area outside the forest (100% arrangement for the small-seeded species was the irradiance). same, but Musanga had 40 seeds per dish (n = 160) Eleven species were tested in two batches, in the and Nauclea had only three dishes (n = 75). rainy seasons of 1992 and 1993. In each replicate, 25 # 1999 British Germination media were kept moist by regular seeds of each species were planted in forest topsoil Ecological Society Journal of Ecology, watering, and germination was recorded at 3-day in bowls protected with 1-cm mesh chicken wire. 87, 772±783 intervals. The dark and low red : far-red treatments Freshly collected seeds were pressed half-way into 776 the soil and subsequent germination monitored at with low water content and the bigger seeds Light and weekly intervals between mid-May and early included some of the higher water contents, but the germination of October in 1992 and April±June in 1993. Water was correlation was not signi®cant. Wind-dispersed spe- forest trees provided only by natural wet season rainfall. cies were generally of moderate mass, and pioneers Seed germination and seedling biomass accumula- were more common among small-seeded species, tion in forest shade (2% irradiance) and in a gap with the notable exception of Ricinodendron heudelo- (30% irradiance) was assessed in two species, the tii, which had the second most massive seed at 1.6 g. pioneer Ceiba pentandra and the non-pioneer light Larger seeds are known in West African rain forest demander Pericopsis elata, by planting seeds in tree species [e.g. Okoubaka aubrevillei (c. 100 g fresh bowls as in the previous experiment and taking weight), Balanites wilsoniana (c. 50 g), Mammea weekly seedling harvests for 7 weeks after germina- africana (38 g) and Tieghemella heckelii (19 g)] but tion. Harvested seedlings were dried to constant few are smaller than those of Nauclea (0.0003 g). weight and dry mass of the whole seedling recorded.

GERMINATION IN LIGHT AND DARK, AND STATISTICAL ANALYSIS IN NEUTRAL AND GREEN SHADE Testing for di€erences in percentage germination employed chi-squared tests on raw counts with Of 17 species tested in the shadehouse experiments, results pooled for bowls/replicates within a treat- only the three with the smallest seeds showed signi®- ment. Mean days to germinate were compared with cant di€erences in percentage germination between t-tests (the 3-day period over which each seed germi- light and dark: germination was very low or zero in nated was recorded). darkness but appreciable in 5% irradiance (Table 2 and Fig. 1). Musanga, Nauclea and Milicia are com- mon in forest soil seed banks (Bouharmont 1954; Results Hall & Swaine 1980) and their seeds develop in large numbers in ¯eshy, scented fruits, and are prob- SEED CHARACTERISTICS ably dispersed by bats. Several of the species that Relationships among seed characters in Table 1 were are widely regarded as pioneers (Hawthorne 1995), not strong. The smallest-seeded species had seeds notably the two forest species of Terminalia, Ceiba

Table 2 E€ects of light (30% irradiance) vs. dark and neutral (R:FR = 0.83) vs. green (R:FR = 0.43) shade on the germina- tion of tree species in shadehouses. Di€erences between pairs of treatments are signi®cant (w2) at: **P < 0.01; ***P < 0.001; or not signi®cant (NS)

Mean percentage germination Mean days to germinate

Neutral Green Light Dark shade shade Light Dark Species Irradiance (%) 30 0 5 5 30 0

Blighia sapida 100 NS 98 93 NS 98 8 * 7 Ricinodendron heudelotii 33 NS 42 32 NS 28 42 ** 35 Pterygota macrocarpa 71 NS 73 65 NS 70 56 NS 51 Guarea cedrata 71 NS 70 74 NS 71 ± ± Entandrophragma utile 77 NS 83 77 NS 75 27 *** 23 Sterculia rhinopetala 52 NS 57 ± ± 10 NS 10 Khaya anthotheca 51 NS 47 ± ± 17 NS 17 Pericopsis elata 69 NS 59 69 NS 66 16 *** 9 Mansonia altissima 80 NS 81 76 NS 79 21 *** 16 Lovoa trichilioides 89 NS 93 94 NS 92 ± ± Khaya ivorensis 68 NS 73 64 NS 74 26 *** 22 Terminalia ivorensis 43 NS 37 34 NS 33 66 NS 64 Terminalia superba 77 NS 77 69 NS 72 25 ** 23 Ceiba pentandra 56 NS 53 53 NS 52 25 *** 19 Celtis mildbraedii 71 NS 70 67 NS 65 21 ** 19 Funtumia elastica 63 NS 66 66 NS 60 28 NS 28 Milicia excelsa 33 + *** 3 33 NS 30 ± 20 Musanga cecropioides 78 + *** 0 78 NS 77 ± ± # 1999 British Nauclea diderrichii 37 + ** 7 37 *** 15 ± 24 Ecological Society Journal of Ecology, + 5% irradiance. 87, 772±783 ± Not recorded or not tested. 777 In the growth chamber tests on two of the photo- B. Kyereh, blastic species, the interaction between irradiance M.D. Swaine & and R:FR ratio was examined at constant tempera- J. Thompson ture. In both Nauclea and Musanga, germination increased with irradiance (Table 3). Low R:FR light had no e€ect on germination at 5 or 30 mmol m±2 s±1 irradiance, but signi®cantly depressed germination in both species at 1 mmol m±2 s±1 irradiance. Thus the e€ects of the low energy reaction were only evi- dent when irradiance was low and the high irradi- ance response, which may inhibit germination (Salisbury & Ross 1978), was muted. The implica- tion is that in forest shade, where irradiance is low, the seeds of these pioneers are more likely to remain dormant, but will germinate in even small canopy gaps with only 5 mmol m±2 s±1.InMusanga, germina- tion at 0.1 mmol m±2 s±1 only occurred at a high R:FR ratio, but even then was very low (three seeds Fig. 1 Germination (%) of freshly collected seeds of 19 of 120). Ghanaian rain forest tree species in light [30% irradiance, except Milicia, Musanga and Nauclea (5%)] and dark treat- ments of the shadehouse experiment. The diagonal line shows equality of germination in light and dark. Species EFFECTS OF IRRADIANCE IN SHADEHOUSE classi®ed a priori as pioneers (Hawthorne 1995) are shown EXPERIMENTS as open circles and named in bold face. Full species names as in Table 1. Five species representing a range of guilds were tested for the e€ect of irradiance on percentage ger- mination by planting seeds in shadehouses with 2%, 30% and 65% irradiance. Two of the non-pioneers (Guarea cedrata and Pterygota macrocarpa) were pentandra and Ricinodendron heudelotii, were not una€ected by di€erences in irradiance, but the other responsive to light, which seems to con®rm that three species showed contrasting responses to photoblasticity is characteristic only of a subset of increased irradiance (Table 4). Germination was the pioneer guild. enhanced by high irradiance in the non-pioneer In the shadehouse experiment, there was no e€ect Pericopsis elata and in Ricinodendron, and depressed of low red : far-red ratio (R:FR) at low irradiance in Terminalia ivorensis.InRicinodendron, the species (5%) for any species, including those shown to be with extended germination, ungerminated seeds photoblastic above, with the exception of Nauclea were tested for viability using tetrazolium chloride. diderrichii in which germination was reduced by A high proportion (91%) of the seeds that failed to more than 50% (Table 2). The R:FR quotient used germinate in 2% irradiance remained viable, sug- was 0.43, a little higher than would be typical of gesting that the ungerminated seeds had some closed forest understorey. Thus it is possible that a requirement for radiant energy for germination, lower value might have elicited more di€erences although no such e€ect had been suggested by the among the species (Va zquez-Ya nes & Smith 1982). results of the previous light/dark experiment.

Table 3 E€ect of irradiance and R:FR ratio on percentage germination (n = 120 per treatment) in two photoblastic tree spe- cies at constant temperature (27 C). ±, not tested. Signi®cance (w2) between rows and between columns are: **P < 0.01; ***P < 0.001; not signi®cant (NS)

Irradiance (mmol m±2 s±1)

R:FR 30 5 1 0.1

Musanga cecropioides 0.83 87 NS 93 *** 71 *** 2 0.43 89 NS 87 *** 35 *** 0 P NS NS *** # 1999 British Nauclea diderrichii 0.83 ± 96 ** 85 ± Ecological Society 0.43 ± 96 *** 68 ± Journal of Ecology, P NS ** 87, 772±783 778 Table 4 Percentage germination in three shadehouses with di€ering irradiance. Pioneer species in bold. ±, not tested Light and Irradiance (%) germination of forest trees Species 2 30 65 Probability (w2)

Guarea cedrata 56 67 61 NS Pterygota macrocarpa 79 ± 84 NS Pericopsis elata 69 ± 100 0.001 Terminalia ivorensis 42 42 19 0.001 Ricinodendron heudelotii 0 11 34 0.001 Viability of ungerminated Ricinodendron seeds 91 67 30

GERMINATION IN FOREST CONDITIONS forest (Table 5) experiments. Terminalia ivorensis showed signi®cant depression of germination in high The small-seeded photoblastic species were not irradiance in both environments, but the reduced tested in the forest experiments, but three pioneers germination observed in forest shade had not been according to Hawthorne (1995) were included recorded in the 2% shadehouse. In the forest, (Table 5). Germination in the forest understorey Pericopsis did not show the increased germination at (mean irradiance, 2%) was less in these three pio- high irradiance that was recorded in the shadehouse, neers than in any of the non-pioneers. Terminalia and Pterygota showed reduced germination outside ivorensis showed only 12% germination in deep the forest but not in the 65% shadehouse. Some of shade, about a third of its maximum (in 30% irradi- these discrepancies may be attributed to desiccation ance), while for the other two pioneers germination in the forest, where seeds were not watered, com- in shade was near the maximum value for the spe- pared with the shadehouse experiment, in which the cies. seeds were kept moist (Orozco-Segovia & Va zquez- All but two species showed signi®cant di€erences Ya nes 1990). in percentage germination among the forest sites. In most, these di€erences were substantial and largely SPEED OF GERMINATION due to depression of germination in 100% irradiance relative to that in 2% (Fig. 2). Terminalia ivorensis The distribution of germination day was unimodal was notable for signi®cantly greater germination in for all species (except for Ricinodendron in light), so intermediate irradiances, while Blighia sapida, which that the mean day of germination could be used as a has a large, black seeds with high water content, measure of rate. The mean day was generally less in was una€ected by gap size. These results did not darkness than in the light in the shadehouse experi- agree in all cases between shadehouse (Table 4) and ments (Table 2), but the e€ect was generally small

Table 5 Percentage germination and rate of germination (mean day of germination) in forest understorey (2% irradiance), canopy gaps of di€erent size (15%, 30%, 50% irradiance) and outside the forest (100%). Species are ordered by percentage germination in 2% irradiance; pioneers (Hawthorne 1995) in bold. Signi®cance of di€erences within species are: *P < 0.05; **P < 0.01; ***P < 0.001; not signi®cant (NS)

Percentage germination Mean days to germinate Irradiance (%) Irradiance (%)

Species 2 15 30 50 100 w2 2 15 30 50 100 Mean

Terminalia ivorensis 12 23 37 33 19 22.3 *** 79 55 41 37 33 61.3 Ceiba pentandra 57 40 55 60 42 13.4 ** 19 19 15 16 13 20.5 Terminalia superba 68 66 75 63 55 9.4 * 25 20 20 30 58 38.3 Khaya anthotheca 73 66 68 57 10 106.7 *** 24 27 30 34 70 46.3 Pterygota macrocarpa 75 80 87 87 57 34.8 *** 90 85 100 86 81 110.5 Entandrophragma utile 77 85 88 88 18 176.5 *** 29 29 30 33 66 46.8 Celtis mildbraedii 79 75 83 79 44 50.2 *** 23 23 22 21 34 30.8 Albizia ferruginea 80 72 85 85 74 8.9 NS 23 27 26 26 27 32.3 # 1999 British Pericopsis elata 83 43 75 80 72 49.3 *** 16 12 17 15 20 20.0 Ecological Society Blighia sapida 94 96 97 98 98 3.4 NS 18 17 18 16 13 20.5 Journal of Ecology, Mansonia altissima 95 96 92 82 17 251.4 *** 19 19 18 24 48 32.0 87, 772±783 779 B. Kyereh, M.D. Swaine & J. Thompson

Fig. 2 Germination in forest environments of di€ering irradiance of 11 tree species (codes as in Table 1) expressed as a pro- portion of germination in deep forest shade (2% irradiance). Species are ordered by germination in 100% irradiance. Signi®cance of di€erence among irradiances (w2) are: NS, not signi®cant; *P < 0.05; **P < 0.001; ***P < 0.001.

compared with di€erences among species. In the for- slower than those in the shadehouse. On average, est experiments, some species were considerably seeds planted in the forest took about 2 weeks longer slower to germinate in 100% irradiance than in to complete germination than in the shadehouse, shade, but the e€ect was not consistent among spe- presumably due to slower imbibition. These rela- cies (Table 5). These e€ects were probably due in tionships were used to estimate forest germination part to slower imbibition at higher irradiance, espe- rates for those species that were tested only in the cially in unwatered treatments, interacting with dif- shadehouse. When species were ordered by the ferences in species' abilities to remain viable. mean number of days (observed or predicted) to The mean day of germination and the number of complete germination in the forest, as in Fig. 3, the days to complete germination were highly correlated ranking was very similar to that for mean day of in both shadehouse experiments (r = 0.973, germination. There was considerable variation d.f. = 15, P < 0.001) and in the forest (r = 0.976, among species, germination being complete in d.f. = 9, P < 0.001), suggesting that either measure Blighia in about 3 weeks but taking nearly 6 months is a robust indication of a species' rate of germina- in Pterygota. The rate of germination showed no tion. signi®cant relationship with seed size, moisture con- In addition, the mean day of germination (and tent or photoblasticity (Tables 1 and 2). days to complete germination) was correlated Ricinodendron was the only species to show bimo- between shadehouse and forest experiments dal distribution of germination, and then only in (r = 0.817 and 0.788, respectively; d.f. = 8, P < 0.01 lighted treatments. In 30% neutral irradiance in the for each), but rates in the forest were consistently shadehouse, the ®rst phase of germination started

# 1999 British Ecological Society Fig. 3 Rate of germination (mean day of germination, shaded columns; days to complete germination, open columns) in Journal of Ecology, forest conditions for 18 tree species (codes in Table 1). The values are the means of measurements in several treatments, and 87, 772±783 those marked `e' are estimated for the forest from shadehouse results. Species are ordered by days to complete germination. 780 Light and germination of forest trees

Fig. 4 Changes in seedling biomass over 7 weeks after germination in forest shade (2% irradiance, ®lled symbols) and in a small canopy gap (30%, open symbols) for the pioneer Ceiba pentandra (circles) and the non-pioneer light-demander, Pericopsis elata (squares). Fitted lines are exponential (in gaps) and linear (in shade).

27 days after planting and ended 21 days later. Discussion Germination resumed after an interval of 28 days and ceased 90 days after planting. A similar pattern Substantial di€erences exist among the seed charac- was recorded in the low R:FR treatment, but not in teristics of the West African tree species tested in darkness where germination was continuous and these experiments. Seed fresh mass varies by an completed after 41 days, achieving a higher ®nal ger- order of four, seed water content by a factor of 12 mination. Ungerminated seeds in the dark treatment and days to complete germination in forest condi- showed high viability with the tetrazolium chloride tions by a factor of six. None of these are correlated test, and germinated later in light (Table 4). among themselves, nor with percentage germination in the forest. Percentage germination varies among species, but it is dicult to propose species-speci®c rates because of the unknown quality of the seed collections and because variation in incident radiation has a marked BIOMASS ACCUMULATION OF YOUNG in¯uence on percentage germination for several spe- SEEDLINGS IN FOREST CONDITIONS cies. The relationships with irradiance are thought To test the hypothesis that some pioneers fail to generally to be due to indirect e€ects on seed tem- establish in forest shade because of a negative car- perature, or more probably seed moisture content, bon balance, rather than an inability to germinate in rather than a light e€ect because only three species shade, two species were planted in forest shade (2% showed a photoblastic response in the light/dark irradiance) and in a small canopy gap (30% irradi- experiment, and only one showed an e€ect of low ance). Ceiba pentandra is a well-known pioneer, and R:FR ratio at low irradiance in the shadehouse although Hawthorne (1995) calls Pericopsis elata a (Table 2). non-pioneer light-demander, it was regarded by Hall The growth chamber experiment with Musanga & Swaine (1981) as a pioneer. and Nauclea (Table 3) showed that an e€ect of a low In the small gap, both species showed positive R:FR ratio was only detectable at irradiances less biomass accumulation, following exponential trends than 5 mmol m±2 s±1 (which is < 0.25% of a conser- (Fig. 4), with the pioneer, Ceiba, growing fastest. In vative value for full irradiance of 2000 mmol m±2 deep shade, however, both Ceiba and Pericopsis lost s±1). As the shadehouse light quality experiment was biomass, following linear trends. After 7 weeks, all conducted at 5% irradiance we should not be sur- seedlings of Ceiba in shade had collapsed due to fail- prised to see no e€ect in Musanga or Milicia. For # 1999 British ure of the stem above the hypocotyl. At this time Musanga at least, the low energy reaction appears to Ecological Society ±2 ±1 Journal of Ecology, seedling dry mass had fallen to 60% of the value 1 be irrelevant at irradiances < 1 mmol m s , sug- 87, 772±783 week after germination. gesting that germination in the forest in these photo- 781 blastic species will be depressed only in the darkest study, particularly because temperature was not B. Kyereh, corners, or if the seed is buried in the soil. fully controlled in the shadehouse experiments. M.D. Swaine & The very low threshold for light-mediated in¯u- All seeds used in these experiments were freshly J. Thompson ences on germination leads us to expect that germi- collected and generally showed good viability. nation in the forest will be at or near maximum in Va zquez-Ya nes & Orozco-Segovia (1990) report the deep shade treatments (2% irradiance), as is gen- that most tropical tree species germinate freely when erally the case in Table 5. For the photoblastic spe- freshly collected, including most pioneers, but dor- cies, none of which was tested in forest conditions, mancy may be subsequently imposed or induced (or we predict that dispersed seed will germinate in deep viability lost) if germination is prevented by a lack forest shade providing it is not buried in the soil or of water, by storage or by dispersal to forest shade covered by litter. The e€ects of increasing canopy with a low R:FR light. We have no direct informa- opening on seed germination are somewhat varied, tion on these processes for our species but our dif- but the most common response is a depression of ferences in rates of germination are relevant for germination in open conditions (Fig. 2). This e€ect successful establishment of seedlings in forest. Most does not appear to be due to desiccation as it is not species seeds are dispersed in the dry season, and stronger in seeds with high water content, which can must wait for variable periods before rainfall is su- be killed by relatively small losses of moisture cient to permit imbibition (Garwood 1983). It is evi- (Baskin & Baskin 1998). Blighia, the largest seeded- dent from the duration of germination in Fig. 4 that species, has the second highest water content and a most species have the capacity to remain viable for black seed coat and showed no response to irradi- at least 1 month, and, in 10 species, for 2 or more ance, maintaining high germination (> 94%) in all months. sites. Two factors may assist Blighia: it has the fast- The results presented here argue against the idea est rate of germination, reducing the opportunity for that the pioneer guild, as presently recognized, may desiccation, and is unusual among forest species in be de®ned solely by gap-dependent germination. dispersing its seeds in the relatively cloudy and cool The two species tested showed a negative carbon wet season. Pioneers were no more resistant to the balance in forest shade, suggesting that this limita- e€ect of high irradiance than non-pioneers: Ceiba tion may be the more ubiquitous cause of the failure and Terminalia superba both showed depression of of pioneers to establish in forest shade. Only three germination at high irradiance, as did Terminalia species showed a photoblastic response, and growth ivorensis, although germination in this species was chamber tests indicated that this is only a€ected at even more reduced by the lowest irradiance irradiances less than those normally found in forest (Table 5). shade. Daily temperature range and maximum also The pioneer Euphorb Ricinodendron heudelotii change markedly with canopy opening, as well as stands out among the species tested for its rather the availability of water at the soil surface, and the inconsistent responses. It was not photoblastic in interaction of these factors with irradiance needs to the light/dark experiment, was una€ected by be investigated. Evidently photoblasticity is a char- reduced R:FR light, but responded strongly to dif- acteristic of a subset of pioneers, and is associated ferences in irradiance (Table 4). We may ask how here with small-seeded, ¯eshy-fruited species that germination can be so high in darkness (42%) if it is are found in the soil seed bank. This is a useful sub- zero in the 2% shadehouse? The main di€erence division of the guild, but it would seem impractical between the treatments is that the irradiance tests to rede®ne pioneers on this basis because few species were done in open bowls rather than enclosed seed have been tested experimentally and because the trays, so that a temperature e€ect is a strong possi- existing de®nition is useful and widely applicable. It bility. Temperatures within the enclosed seed trays seems probable that the photoblastic group will be were 4 C higher than in the 2% shadehouse. relatively small, and include particularly the small Temperature commonly interacts with other envir- stature genera such as Musanga, some Ficus, onmental variables to a€ect germination (Mayer & Cecropia, Trema, and Harungana. Poljako€-Mayber 1975; Baskin & Baskin 1998). For Preservation of the current suite of pioneer species example, Chamshama & Downs (1982; in Baskin & thus depends in most cases on their inability to Baskin 1998) described the interaction between light grow in forest shade, as has been con®rmed here for and temperature for the photoblastic Chlorophora two species, Pericopsis and Ceiba. Experiments have excelsa (= Milicia excelsa; Table 2). They reported shown that other West African species also have that at a constant temperature of 30 C, light negative growth rates in low irradiance. Agyeman et reduced germination to 3% compared with 37% in al. (1999); Swaine et al. (1997) showed that relative the dark, but at alternating temperatures of 30/ growth rate in established seedlings was negative in # 1999 British 20 C, germination in light and dark was similar a 2% irradiance shadehouse in Mansonia altissima, Ecological Society Journal of Ecology, (45±50%). The interaction of temperature and light Milicia excelsa, Ricinodendron heudelotii, Ceiba pen- 87, 772±783 for our West African tree species needs further tandra and Sterculia rhinopetala. This was con®rmed 782 in forest shade (2% irradiance) for Ceiba and Hawthorne, W.D. (1993) Forest Regeneration after Light and Mansonia (Swaine et al. 1997). To place the de®ni- Logging. ODA Forestry Series no. 3. Natural Resources Institute, Chatham Maritime. germination of tion of pioneers on a more objective basis by such Hawthorne, W.D. (1995) Ecological Pro®les of Ghanaian forest trees means is, however, dicult because it requires the Forest Trees. Tropical Forestry Papers 29. Oxford selection of an arbitrary threshold of irradiance, Forestry Institute, Oxford, UK. with attendant problems of measurement, and the Kennedy, D.K. & Swaine, M.D. (1992) Germination and use of consistent experimental conditions across dif- growth of colonizing species in arti®cial gaps of di€er- ferent continents. ent sizes in dipterocarp rain forest. Philosophical Transactions of the Royal Society Series B, 335, 357± 367. Acknowledgements Li, M., Lieberman, M. & Lieberman, D. (1996) Seedling demography in undisturbed tropical wet forest in We thank the Director of the Forestry Research Costa Rica. Ecology of Tropical Forest Tree Seedlings Institute of Ghana, Dr A. Ofusu Asiedu, for his (ed. M.D. Swaine), pp. 285±314. MAB Series, Vol. 17. UNESCO/Parthenon, Paris/Carnforth. encouragement and ®nancial support of this Mayer, A.M. & Poljako€-Mayber, A. (1975) The research. The University of Science and Technology Germination of Seeds. Pergamon Press, Oxford, UK. Institute of Renewable Natural Resources, directed Ng, F.S.P. (1980) Germination ecology of Malaysian by Mr J.G.K. Owusu, also provided support. The woody plants. Malaysian Forester, 43, 406±437. research was also funded by the Overseas Orozco-Segovia, & Va zquez-Ya nes (1989) Light e€ect on Development Authority (now the Department for seed germination in Piper L. Acta Oecologia Plantarum, 10, 125±146. International Development) through its bilateral aid Orozco-Segovia, & Va zquez-Ya nes (1990) E€ect of moist- programme. We are grateful to Mrs A. Gyimah for ure on longevity in seeds of some rain forest species. her advice and the support of her Seed Technology Biotropica, 22, 215±216. group. Dr E.M. Veenendaal was always interested Raich, J.W. & Gong, W.K. (1990) E€ects of canopy open- and helpful. ing on tree seed germination in a Malaysian diptero- carp forest. Journal of Tropical Ecology, 6, 203±217. Roberts, E.H. (1973) Predicting the storage life of seed. 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# 1999 British Ecological Society Journal of Ecology, 87, 772±783